Receptive-field construction in cortical inhibitory interneurons.

In the somatosensory 'barrel' cortex (where each barrel represents an individual whisker) the receptive fields of cortical spiny neurons show considerable specificity for the direction of whisker displacement, as do the receptive fields of thalamocortical (TC) neurons that provide input to the barrels. In contrast, putative fast-spike inhibitory interneurons in layer 4 of the barrel cortex lack directional preference, but are exquisitely sensitive to low stimulus intensities. Here we show, in adult rabbits, that these sensitive and broadly tuned inhibitory receptive fields are generated by an unselective pooling of convergent functional inputs from topographically aligned TC neurons with very diverse response properties.

The impact of 'bursting' thalamic impulses at a neocortical synapse.

Considerable effort has gone into understanding the mechanisms underlying high-frequency 'bursting' of thalamocortical impulses, their sensory information content and their involvement in perception. However, little is known about the influence of such impulses on their cortical targets. Here we follow bursting thalamic impulses to their terminus at the thalamocortical synapse of the awake rabbit, and examine their influence on a class of somatosensory cortical neurons. We show that thalamic bursts potently activate cortical circuits. Initial impulses of each burst have a greatly enhanced ability to elicit cortical action potentials, and later impulses in the burst further raise the probability of eliciting spikes. In some cases, multiple cortical spikes result from a single burst. Moreover, we show that the interval preceding each burst is crucial for generating the enhanced cortical response. The powerful activation of neocortex by thalamocortical bursts is fully consistent with an involvement of these impulses in perceptual/attentional processes.

Role of different sensory inputs for maintenance of body posture in sitting rat and rabbit.

In this paper, we describe the postural activity in sitting rats and rabbits. An animal was positioned on the platform that could be tilted in the frontal plane for up to +/-20-30 degrees, and postural corrections were video recorded. We found that in both rat and rabbit, the postural reactions led to stabilization of the dorsal-side-up trunk orientation. The result of this was that the trunk tilt constituted only approximately 50% (rat) and 25% (rabbit) of the platform tilt. In addition, in the rabbit the head orientation was also stabilized. Trunk stabilization persisted in the animals subjected to the bilateral labyrinthectomy and blindfolding, suggesting that the somatosensory input is primarily responsible for trunk stabilization. Trunk stabilization was due to extension of the limbs on the side moving down, and flexion of the opposite limbs. EMG recordings showed that the limb extension was caused by the active contraction of extensor muscles. We argue that signals from the Golgi tendon organs of the extensor muscles may considerably contribute to elicitation of postural corrective responses to the lateral tilt.

The influence of single VB thalamocortical impulses on barrel columns of rabbit somatosensory cortex.

Extracellular recordings were obtained from single neurons in ventrobasal (VB) thalamus of awake rabbits while field potentials were recorded at various depths within topographically aligned and nonaligned barrel columns of somatosensory cortex (S1). Spike-triggered averages of cortical field potentials were obtained following action potentials in thalamic neurons. Action potentials in a VB neuron elicited a cortical response within layer 4 with three distinct components. 1) A biphasic, initially positive response (latency <1 ms) was interpreted to reflect activation of the VB axon terminals (the AxTP). This response was not affected by infusion of an alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA)/kainate receptor antagonist within the barrel. In contrast, later components of the response were completely eliminated and were interpreted to reflect focal synaptic potentials. 2) A negative potential [focal synaptic negativity (FSN)] occurred at a mean latency of 1.65 ms and lasted approximately 4 ms. This response had a rapid rise time ( approximately 0.7 ms) and was interpreted to reflect monosynaptic excitation. 3) The third component was a positive potential (the FSP), with a slow rise time and a half-amplitude duration of approximately 30 ms. The FSP showed a weak reversal in superficial cortical layers and was interpreted to reflect di/polysynaptic inhibition. The amplitudes of the AxTP, the FSN, and the FSP reached a peak near layer 4 and were highly attenuated in both superficial and deep cortical layers. All components were attenuated or absent when the cortical electrode was missaligned from the thalamic electrode by a single cortical barrel. Deconvolution procedures revealed that the autocorrelogram of the presynaptic VB neuron had very little influence on either the amplitude or duration of the AxTP or the FSN, and only a minor influence (mean, 11%) on the amplitude of the FSP. We conclude that individual VB thalamic impulses entering a cortical barrel engage both monosynaptic excitatory and di/polysynaptic inhibitory mechanisms. Putative inhibitory interneurons of an S1 barrel receive a highly divergent/convergent monosynaptic input from the topographically aligned VB barreloid, and this results in sharp synchrony among these interneurons. We suggest that single-fiber access to disynaptic inhibition is facilitated by this sharp synchrony, and that the FSP reflects a consequent synchronous wave of feed-forward inhibition within the S1 barrel.

Descending corticofugal neurons in layer 5 of rabbit S1: evidence for potent corticocortical, but not thalamocortical, input.

Extracellular recordings were obtained from descending corticofugal neurons of layer 5 (CF-5 neurons) in primary somatosensory cortex (S1) of awake rabbits. These cells were identified by antidromic activation via stimulation sites in ventrobasal (VB) thalamus. Recordings were also obtained from putative GABA-ergic interneurons (suspected inhibitory interneurons, SINs) located in the same microelectrode penetrations, and in close proximity (+/- 300 microns) to the CF-5 neurons. In some experiments, the above populations were recorded simultaneously with neurons in the topographically aligned VB thalamic barreloid. Each of several experimental strategies failed to reveal evidence of monosynaptic thalamic input to CF-5 neurons, but revealed a clear monosynaptic input to neighboring SINs: (1) whereas CF-5 neurons responded at very long synaptic latencies to intense electrical stimulation of VB thalamus, neighboring SINs responded at short latencies; (2) whereas cross-correlations between CF-5 neurons and topographically aligned VB neurons failed to show significant peaks indicative of monosynaptic VB input, neighboring SINs did show such peaks; and (3) whereas CF-5 neurons were unresponsive to microstimulation of topographically aligned VB thalamic barreloids, neighboring SINs were very responsive to such stimulation. Both CF-5 neurons and neighboring SINs responded to electrical stimulation of the corpus callosum with a robust, short-latency synaptic response. This finding demonstrates that CF-5 neurons are capable of vigorous, short-latency responses to excitatory synaptic input. These data suggest considerable specificity in the thalamocortical connectivity of subpopulations within layer 5, and support the notion that CF-5 neurons are dominated by corticocortical rather than thalamocortical input.

Sharp, local synchrony among putative feed-forward inhibitory interneurons of rabbit somatosensory cortex.

Many suspected inhibitory interneurons (SINs) of primary somatosensory cortex (S1) receive a potent monosynaptic thalamic input (thalamocortical SINs, SINstc). It has been proposed that nearly all such SINstc of a S1 barrel column (BC) receive excitatory synaptic input from each member of a subpopulation of neurons within the topographically aligned ventrobasal (VB) thalamic barreloid. Such a divergent and convergent network leads to several testable predictions: sharply synchronous activity should occur between SINstc of a BC, sharp synchrony should not occur between SINstc of neighboring BCs, and sharp synchrony should not occur between SINs or other neurons of the same BC that do not receive potent monosynaptic thalamic input. These predictions were tested by cross-correlating the activity of SINstc of the same and neighboring BCs. Correlations among descending corticofugal neurons of layer 5 (CF-5 neurons, identified by antidromic activation) and other neurons that receive little or no monosynaptic VB input also were examined. SINs were identified by a high-frequency (>600 Hz) burst of three or more spikes elicited by VB stimulation and had action potentials of short duration. SINstc were further differentiated by short synaptic latencies to electrical stimulation of VB thalamus (<1.7 ms) and to peripheral stimulation (<7.5 ms). The above predictions were confirmed fully. 1) Sharp synchrony (+/-1 ms) was seen between all SINstc recorded within the same BC (a mean of 4.26% of the spikes of each SINtc were synchronized sharply with the spikes of the paired SINtc). Sharp synchrony was not dependent on peripheral stimulation, was not oscillatory, and survived general anesthesia. Sharp synchrony was superimposed on a broader synchrony, with a time course of tens of milliseconds. 2) Little or no sharp synchrony was seen when CF-5 neurons were paired with SINstc or other neurons of the same BC. 3) Little or no sharp synchrony was seen when SINstc were paired with other SINstc located in neighboring BCs. Intracellular recordings obtained from three SINs in the fully awake state supported the assertion that SINs are GABAergic interneurons. Each of these cells met our extracellular criteria for identification as a SIN, each had a spike of short duration (0.4-0.5 ms), and each responded to a depolarizing current pulse with a nonadapting train of action potentials. These results support the proposed network linking VB barreloid neurons with SINstc within the topographically aligned BC. We suggest that sharp synchrony among SINstc results in highly synchronous inhibitory postsynpatic potentials (IPSPs)in the target neurons of these cells and that these summated IPSPs may be especially effective when excitatory drive to target cells is weak and asynchronous.

Neocortical efferent neurons with very slowly conducting axons: strategies for reliable antidromic identification.

Although simple in concept, reliable antidromic identification of efferent populations poses numerous technical challenges and is subject to a host of sampling biases, most of which select against the detection of the neurons with slowly conducting axons. This problem is particularly acute in studies of the neocortex. Many neocortical efferent systems have large sub-populations with very slowly conducting, nonmyelinated axons and these elements have been relatively neglected in antidromic studies of neocortical neurons. The present review attempts to redress this problem by analyzing the steps that must necessarily precede antidromic identification and the sampling biases associated with each of these steps. These steps include (1) initial recognition that the microelectrode is near a neuron; (2) activation of the efferent axon via the stimulating electrode; (3) conduction of the antidromic impulse from stimulation site to soma; (4) detection of the antidromic spike in the extracellular record and (5) discriminating antidromic from synaptic activation. Experimental strategies are suggested for minimizing the sampling biases associated with each of these steps; most of which can be reduced or eliminated by appropriate experimental procedures. Careful attention to such procedures will make it possible to better understand the nature and function of the information flow along the very slowly conducting axonal systems of the neocortex.

Subthreshold receptive fields and baseline excitability of "silent" S1 callosal neurons in awake rabbits: contributions of AMPA/kainate and NMDA receptors.

The contribution of NMDA and non-NMDA receptors to excitatory subthreshold receptive fields was examined in callosal efferent neurons (CC neurons) in primary somatosensory cortex of the fully awake rabbit. Only neurons showing no traditional (suprathreshold) receptive fields were examined. Subthreshold responses were examined by monitoring the thresholds of efferent neurons to juxtasomal current pulses (JSCPs) delivered through the recording microelectrode. Changes in threshold following a peripheral conditioning stimulus signify a subthreshold response. Using this method, excitatory postsynaptic potentials and inhibitory postsynaptic potentials are manifested as decreases and increases in JSCP threshold, respectively. NMDA and non-NMDA agonists and antagonists were administered iontophoretically via a multibarrel micropipette assembly attached to the recording/stimulating microelectrode. Receptor-selective doses of both AMPA/kainate and NMDA antagonists decreased the excitability of CC neurons in the absence of any peripheral stimulation. Threshold to JSCPs rose by a mean of 20% for both classes of antagonist. Despite the similar effects of NMDA and non-NMDA antagonists on baseline excitability, these antagonists had dramatically different effects on the subthreshold excitatory response to activation of the receptive field. Whereas receptor-selective doses of AMPA/kainate antagonists either eliminated or severely attenuated the subthreshold excitatory responses to peripheral stimulation, NMDA antagonists had little or no effect on the subthreshold evoked response.

Somatosensory cortical efferent neurons of the awake rabbit: latencies to activation via supra--and subthreshold receptive fields.

1. Latencies to peripheral sensory stimulation were examined in four classes of antidromically identified efferent neurons in the primary somatosensory cortex (S1) of awake rabbits. Both suprathreshold responses (action potentials) and subthreshold responses were examined. Subthreshold responses were examined by monitoring the thresholds of efferent neurons to juxtasomal current pulses (JSCPs) delivered through the recording microelectrode (usually 1-3 microA). Through the use of this method, excitatory postsynaptic potentials (EPSPs) and inhibitory postsynaptic potentials (IPSPs) were manifested as decreases and increases in threshold, respectively. Efferent populations examined included callosal (CC) neurons, ipsilateral corticocortical (C-IC) neurons, and descending corticofugal neurons of layer 5 (CF-5) and layer 6 (CF-6). Very brief air puffs (rise and fall times 0.6 ms) were delivered to the receptor periphery via a high-speed solenoid valve. 2. Whereas all CF-5 neurons had demonstrable suprathreshold excitatory and/or inhibitory responses to peripheral stimulation, most CC, C-IC, and CF-6 neurons did not. CC and CF-6 neurons that yielded no suprathreshold response to the stimulus had lower axonal conduction velocities than those that did respond (P < 0.0001 in both cases). However, subthreshold receptive fields could be demonstrated in many of the otherwise unresponsive CC (81%), C-IC (88%), and CF-6 (43%) neurons. The subthreshold responses usually consisted of an initial excitatory component (a decrease in the threshold to the JSCP) and a subsequent long-duration (> 80 ms) inhibitory component. A few neurons (1 CC, 1 C-IC, and 5 CF-6) showed an initial short latency inhibitory response in the absence of any excitatory component. 3. Some CC and C-IC neurons yielded supra- and/or subthreshold responses to peripheral stimulation at latencies of 6.1-7 ms. All such neurons were found at intermediate cortical depths (thought to correspond to deep layer 2-3 through layer 5). It is argued that such latencies are indicative of monosynaptic activation via thalamic afferents. Very superficial CC and C-IC neurons, and all CF-6 neurons responded to latencies of > 7 ms. All CF-5 neurons responded to latencies of > 8 ms, although many were found at the same depth as the deeper CC and C-IC neurons that responded at monosynaptic latencies. These results indicate that cortical cell type as well as laminar position are important factors that determine the sequence of intracortical neuronal activation after peripheral sensory stimulation.

Cross-correlation and microstimulation: complementary tools in the extracellular analysis of synaptic interactions.

The utility of extracellular microstimulation as an ancillary tool to compliment cross-correlation analyses is explored. This technique aims at demonstrating the "sufficiency' of the spike train generated by the "reference' neuron in eliciting spikes in the "target' neuron. It involves activating the reference neuron with very low-intensity current pulses (1-10 microA) delivered through the recording microelectrode. Microstimulation can provide independent evidence that can either support or refute notions of synaptic connectivity generated by correlation analyses. Data are presented from antidromically identified descending corticofugal neurons and putative inhibitory interneurons of S1 "barrel' cortex of the rabbit and from simultaneously recorded neurons in the topographically aligned "barreloid' of ventroposterior medial thalamus (VPM). A very strong relationship was seen between brief, statistically significant peaks in the cross-correlograms (CCGs) suggestive of monosynaptic excitatory input and the responses of cortical neurons to VPM microstimulation. Thus, 18/19 cortical neurons that responded to microstimulation pulses of < 6 microA showed a significant CCG with the VPM neuron. Conversely, each of 16 cortical neurons that failed to respond at 10 microA also failed to show a significant CCG. CCGs compiled from independent data sets collected before and after hundreds of microstimulation pulses were very similar, showing that such stimulation can be relatively benign. The method has many limitations, which are discussed. The most serious problem is that the effects of extracellular current pulses cannot be limited to the reference neuron. Nevertheless, microstimulation can provide independent experimental support or refutation of hypotheses of synaptic connectivity that are generated by cross-correlation analyses. In addition, since the technique is rapidly implemented and has considerable power to predict significant cross-correlations, it can be useful in deciding which neuron pairs to study when limited time is available for data collection.

Influence of VPM afferents on putative inhibitory interneurons in S1 of the awake rabbit: evidence from cross-correlation, microstimulation, and latencies to peripheral sensory stimulation.

1. Responses of thalamocortical projection neurons and suspected cortical interneurons (SINs) to very brief peripheral stimuli were examined within the vibrissae, the sinus hair, the lip, and the chin representations of ventroposterior medial thalamus (VPM) and primary somatosensory cortex (S1). VPM thalamocortical neurons (N = 40) were identified by their antidromic activation after electrical stimulation of S1. SINs were identified by a high-frequency (> 600 Hz) burst of three or more spikes elicited by suprathreshold stimulation of one or more afferent pathways. SINs also had spikes of very short duration. 2. Previous work has shown that electrical stimulation of VPM elicits a very early and powerful synaptic response in many S1 SINs. Three experimental strategies were employed to test the hypothesis that such responses reflect a monosynaptic VPM input onto SINs and to examine the effects of such input. 1) After a brief peripheral stimulus, the arrival times of VPM thalamocortical impulses in S1 were determined and compared with the initial response times of S1 SINs. 2) Shift-corrected cross-correlograms (CCGs) were constructed from the spike trains of pairs of VPM neurons and SINs that were in precise topographic alignment. 3) Inferences of connectivity based on such CCGs were supported by applying very low-intensity (1-10 microA) microstimulation pulses to the recording microelectrode in VPM and observing evoked responses in the cortical SIN. 3. VPM thalamocortical neurons responded to a brief air puff stimulus at a median latency of 5.05 ms, and the estimated arrival time of the VPM impulses at S1 had a median value of 5.97 ms. This estimate was obtained by adding the antidromic latency of each VPM neuron to the latency of the peripheral stimulus and was supported by similar values obtained from three VPM thalamocortical axons recorded near their termination site within S1. SINs of S1 were among the first cortical neurons to respond to the peripheral stimulus, responding to the air puff at a median latency of 6.6 ms (range 5.7-13.0 ms). The latency of SINs to the peripheral stimulus was strongly related to the latency to gross electrical stimulation of VPM (median value 1.52 ms, r2 = +0.44, P < 0.0001). Many SINs (23 of 34) showed significant shift-corrected CCGs with VPM neurons that were in precise topographic alignment. Most significant CCGs revealed a very brief increase in SIN spike probability (half-amplitude response of approximately 1 ms) that reached a peak value at intervals of 1.4-2.0 ms after the VPM spike.(ABSTRACT TRUNCATED AT 400 WORDS)

Efferent neurons and suspected interneurons in motor cortex of the awake rabbit: axonal properties, sensory receptive fields, and subthreshold synaptic inputs.

1. Properties of antidromically identified efferent neurons within the cortical representation of the vibrissae, sinus hairs, and philtrum were examined in motor cortex of fully awake adult rabbits. Efferent neurons were tested for both receptive field and axonal properties and included callosal (CC) neurons (n = 31), ipsilateral corticocortical (C-IC) neurons (n = 34) that project to primary somatosensory cortex (S-1), and corticofugal neurons of layer 5 (CF-5) (n = 33) and layer 6 (CF-6) (n = 32) that project to and/or beyond the thalamus. Appropriate collision tests demonstrated that substantial numbers of corticocortical efferent neurons project an axon to both the corpus callosum and to ipsilateral S-1. 2. Suspected interneurons (SINs, n = 37) were also studied. These neurons were not activated antidromically from any stimulus site but did respond synaptically to electrical stimulation of the ventrolateral (VL) thalamus and/or S-1 with a burst of three or more spikes at frequencies from 600 to > 900 Hz. All of these neurons also responded synaptically to stimulation of the corpus callosum. The action potentials of these neurons were much shorter in duration (mean = 0.48 ms), than those of efferent neurons (mean = 0.90 ms). 3. CF-5 neurons differed from CC, C-IC, and CF-6 neurons in their spontaneous firing rates, axonal properties, and receptive field properties. Whereas CF-5 neurons had a mean spontaneous firing rate of 4.1 spikes/s, CC, C-IC, and CF-6 neurons all had mean values of < 1 spike/s. Axonal conduction velocities of CF-5 neurons were much higher (mean = 12.76 m/s) than either CC (1.47 m/s), C-IC (0.97 m/s), or CF-6 (mean = 1.96 m/s) neurons. A decrease in antidromic latency (the "supernormal" period) followed a single prior impulse in most CC, C-IC, and CF-6 neurons but was minimal or absent in CF-5 neurons. Although all but two CF-5 neurons responded to peripheral sensory stimulation, many CC (35%), C-IC (59%), or CF-6 (66%) neurons did not. CC, CF-5, and CF-6 neurons that did not respond to sensory stimulation had significantly lower axonal conduction velocities and spontaneous firing rates than those that responded to such stimulation. 4. Sensory receptive fields of neurons in motor cortex were considerably larger than those observed in S-1 but were similar in size to those seen in secondary somatosensory cortex (S-2).(ABSTRACT TRUNCATED AT 400 WORDS)

Monitoring the excitability of neocortical efferent neurons to direct activation by extracellular current pulses.

1. Extracellular action potentials were recorded from antidromically activated efferent neurons in visual, somatosensory, and motor cortex of the awake rabbit using low-impedance metal microelectrodes. Efferent neurons were also activated by current pulses delivered near the soma [juxtasomal current pulses (JSCPs)] through the recording microelectrode. Action potentials generated by JSCPs were not directly observed (because of the stimulus artifact), but were inferred with the use of a collision paradigm. Efferent populations studied include callosal neurons [CC (n = 80)], ipsilateral corticocortical neurons [C-IC (n = 21)], corticothalamic neurons of layer 6 [CF-6 (n = 57)], and descending corticofugal neurons of layer 5 [CF-5, corticotectal neurons of the visual cortex (n = 48)]. 2. Most CC neurons (45/46) and all C-IC (8/8) and CF-6 neurons (39/39) were directly activated by JSCPs at near-threshold intensities. Some CF-5 neurons (9/38), however, showed evidence of indirect activation. All efferent classes had similar current thresholds (means 1.85-2.10 microA) to direct activation by JSCPs, and thresholds were inversely related to extracellular spike amplitude. For each neuron, the range of JSCP intensities that generated response probabilities of between 0.2 and 0.8 was measured, and this "range of uncertainty" was significantly greater in CF-5 neurons (mean 32.7% of threshold) than in CC (mean 19.0%) or CF-6 (mean 20.4%) neurons. 3. Several factors indicate that the threshold of efferent neurons to JSCPs is very sensitive to excitatory and inhibitory synaptic inputs. Iontophoretic applications of gamma-aminobutyric acid (GABA) increased the threshold to JSCPs, and glutamate reduced the threshold. Electrical stimulation of afferent pathways at intensities just below threshold for eliciting action potentials resulted in a dramatic decrease in JSCP threshold. This initial short-latency threshold decrease was specific to stimulation of particular afferent pathways and is thought to reflect excitability changes associated with EPSPs. Examination of such subliminal responses revealed subthreshold synaptic inputs that were not revealed by examination of all-or-none action potentials. In contrast to the specificity of the short-latency threshold decrease, a long-lasting increase in JSCP threshold was seen in virtually all neurons after stimulation of each of the afferent pathways tested. This increase in threshold usually began 20-40 ms after stimulation, lasted for 100-200 ms, and is thought to reflect excitability changes associated with a long-lasting inhibitory postsynaptic potential (IPSP) seen in many cortical neurons. 4. Many neurons in primary somatosensory cortex of rat, cat, and rabbit have no demonstrable receptive fields.(ABSTRACT TRUNCATED AT 400 WORDS)

Efferent neurons and suspected interneurons in second somatosensory cortex of the awake rabbit: receptive fields and axonal properties.

1. Receptive-field properties of antidromically identified efferent neurons within the representation of vibrissae and sinus hairs above the mouth were examined in secondary somatosensory cortex (S-2) of fully awake adult rabbits. Efferent neurons studied included callosal neurons (CC neurons, n = 88), ipsilateral corticocortical neurons (C-IC neurons, n = 51) that project to primary somatosensory cortex (S-1), and corticofugal neurons of layer 5 (CF-5 neurons, n = 63) and layer 6 (CF-6 neurons, n = 42) that project to and/or beyond the thalamus. Appropriate collision tests demonstrated that substantial numbers of corticocortical efferent neurons (21 of 113 tested) project an axon to both the corpus callosum and to ipsilateral S-1. 2. Suspected interneurons (SINs, n = 62) were also studied. These neurons were not activated antidromically from any stimulus site but did respond synaptically to electrical stimulation of the ventrobasal (VB) thalamus with a burst of three or more spikes at frequencies of 600 to greater than 900 Hz. Most of these neurons also responded synaptically to stimulation of S-1 and the corpus callosum. The action potentials of these neurons were much shorter (mean, 0.49 ms) than those of efferent neurons (mean, 1.01 ms). 3. CF-5 neurons differed from CC, C-IC, and CF-6 neurons in their spontaneous firing rates, axonal properties, and receptive-field properties. Whereas CF-5 neurons had a mean spontaneous firing rate of 5.7 spikes/s, CC, C-IC, and CF-6 neurons all had mean values of less than 1/s. Axonal conduction velocities of CF-5 neurons were much higher (mean, 11.90 m/s) than either CC (mean, 2.63 m/s), C-IC (mean, 0.86 m/s), or CF-6 (mean, 1.73 m/s) neurons. A decrease in antidromic latency (the "supernormal" period), which was dependent on prior impulse activity, was seen in most CC, C-IC, and CF-6 neurons but was minimal or absent in CF-5 neurons of comparable conduction velocity. Although all CF-5 neurons responded to peripheral sensory stimulation, many CC (52%), C-IC (49%), and CF-6 (55%) neurons did not. CC and CF-6 neurons that did not respond to sensory stimulation had significantly lower axonal conduction velocities and spontaneous firing rates than those that responded to such stimulation. Whereas no CC, C-IC, or CF-6 neuron responded synaptically to callosal stimulation, 43% of CF-5 neurons (and 78% of SINs) did so respond. Similar differences in synaptic responsivity to stimulation of S-1 were seen in these populations.(ABSTRACT TRUNCATED AT 400 WORDS)

Efferent neurons and suspected interneurons in S-1 forelimb representation of the awake rabbit: receptive fields and axonal properties.

1. Receptive-field properties of antidromically identified efferent neurons within the cutaneous forelimb representation of primary somatosensory cortex (S-1) were examined in fully awake rabbits. Efferent neurons studied included callosal neurons (CC neurons, n = 52), ipsilateral corticocortical neurons (C-IC neurons, n = 48) that project to or beyond the second somatosensory cortical area (S-2), and corticofugal neurons of layer 5 (CF-5 neurons, n = 97) and layer 6 (CF-6 neurons, n = 59) that project to and/or beyond the thalamus. 2. An additional class of neurons was studied that was not activated antidromically from any stimulus site, but which responded synaptically to electrical stimulation of the ventrobasal (VB) thalamus with a burst of three or more spikes at frequencies of 600 to greater than 900 Hz. Most of these neurons also responded synaptically to stimulation of S-2 and the corpus callosum. The action potentials of these neurons were much shorter (mean = 0.45 ms) than those of efferent neurons (mean = 0.95 ms). Such properties have been associated with interneurons found throughout the central nervous system, and these neurons are thereby referred to as suspected interneurons (SINs). 3. CF-5 neurons differed from CC, C-IC, and CF-6 neurons in their spontaneous firing rates, axonal properties, and receptive-field properties. Whereas CF-5 neurons had a mean spontaneous firing rate of 5.5 spikes/s, CC, C-IC, and CF-6 neurons had mean values of less than 1/s. Axonal conduction velocities of CF-5 neurons were much higher (mean = 12.92 m/s) than either CC (mean = 2.15 m/s), C-IC (mean = 1.31 m/s), or CF-6 (mean = 2.53 m/s) neurons. A decrease in antidromic latency (the "supernormal" period) that was dependent on prior impulse activity was seen in the great majority of CC, C-IC, and CF-6 neurons but was either minimal or absent in CF-5 neurons of comparable conduction velocity. A higher proportion of CF-5 neurons (98%) responded to peripheral sensory stimulation than did either CC (75%), C-IC (71%), or CF-6 (51%) neurons. CF-6 and C-IC neurons that did not respond to sensory stimulation had significantly lower axonal conduction velocities and spontaneous firing rates than those that responded to such stimulation. 4. Cutaneous receptive fields were seen in most neurons that could be driven by peripheral stimulation.(ABSTRACT TRUNCATED AT 400 WORDS)

Efferent neurons and suspected interneurons in S-1 vibrissa cortex of the awake rabbit: receptive fields and axonal properties.

1. The behavioral tractability of the rabbit was exploited and enabled, in the fully awake state, receptive-field analysis of antidromically identified efferent neurons within the vibrissa representation of primary somatosensory cortex (S-1). Efferent neurons studied included ipsilateral corticocortical neurons (C-IC neurons, n = 56) that project to or beyond the second somatosensory cortical area (S-2) and corticofugal neurons of layer 5 (CF-5 neurons, n = 75) and layer 6 (CF-6 neurons, n = 92) that project to and/or beyond the thalamus. 2. An additional class of neurons was studied that was not activated antidromically from any stimulus site, but which responded synaptically to electrical stimulation of the ventrobasal (VB) thalamus with a burst of three or more spikes at frequencies of 600 to greater than 900 Hz. Most of these neurons also responded synaptically to stimulation of S-2. The action potentials of these neurons were much shorter (mean = 0.43 ms), than those of efferent neurons (mean = 0.98 ms). Such properties have been associated with interneurons found throughout the central nervous system, and these neurons are thereby referred to as suspected interneurons (SINs). Although SINs were found at all cortical depths, a strong peak in the distribution occurred just superficial to the peak in the distribution of CF-5 neurons. Most SINs located within this peak responded to deflection of only a single vibrissa. In contrast, SINs located in layer 6 and in layer 2-3 responded to deflection of many vibrissae (median = 11.0 and 5.5 vibrissae, respectively). In addition, SINs of layer 6 and layer 2-3 had significantly longer synaptic latencies to stimulation of VB thalamus than did SINs located at intermediate cortical depths. 3. The properties of efferent neurons and SINs differed considerably. Efferent neurons never responded to stimulation of VB thalamus with the high-frequency burst of spikes characteristic of SINs. Although greater than 70% of CF-6, CF-5 and C-IC neurons had receptive fields that were directionally selective, only 20% of SINs showed any degree of directional selectivity. Furthermore, SINs showed both much lower angular thresholds to vibrissa deflection and a much greater ability to follow high-stimulus frequencies than was seen in efferent neurons. The spontaneous firing rates of SINs had a mean value of 16.5 spikes/s, which was the highest seen in any population within S-1. 4. CF-5 neurons had a number of properties which contrasted with those of both CF-6 and C-IC neurons.(ABSTRACT TRUNCATED AT 400 WORDS)

Efferent neurons and suspected interneurons in binocular visual cortex of the awake rabbit: receptive fields and binocular properties.

1. In fully awake rabbits the stability of the two eyes was monitored and was sufficient to enable receptive-field analysis of antidromically identified efferent neurons and suspected interneurons in the binocular segment of visual area 1. Efferent neurons analyzed included callosal efferent neurons (CC neurons, n = 52), neurons projecting to visual area 2 (CV2 neurons, n = 35), corticotectal neurons (CT neurons, n = 43), and corticogeniculate neurons (CG neurons, n = 51). Six additional neurons projected a branching axon to both the corpus callosum and visual area 2. 2. Most CC and CV2 neurons were found in layer 2-3 and had receptive fields of the simple type. Only two corticocortical neurons with complex receptive fields were found. Orientation tuning ranges of CC and CV2 simple cells were similar and end stopping was prevalent in both CC (62%) and CV2 (45%) neurons. Axonal conduction velocities of CC and CV2 neurons were low (mean = 3.5 and 1.4 m/s, respectively) and visually nonresponsive CC neurons (19%) had conduction velocities that were significantly lower than visually responsive neurons. Spontaneous firing rates of corticocortical neurons were low (mean less than 1 spike/s) and these neurons responded to a lower range of stimulus velocities than did corticofugal neurons. 3. Most CG neurons had simple receptive fields and none had a complex field. Orientation tuning ranges of these neurons were comparable to those of CC and CV2 neurons, but a significantly smaller proportion (12%) were end stopped. Both spontaneous firing rates (mean = less than 1 spike/s) and axonal conduction velocities (mean = 2.4 m/s) of CG neurons were low and, as was found for CC neurons, visually nonresponsive CG neurons (25%) had significantly lower conduction velocities than did visually responsive neurons. 4. CT neurons had receptive fields that were predominantly complex (37%), motion/uniform (28%), or simple (26%). Conduction velocities (mean = 10.9 m/s) and spontaneous firing rates (mean = 7 spikes/s) of CT neurons of all receptive-field types were much higher than those of CC, CV2, and CG neurons. 5. An additional class of neurons was studied that responded synaptically at a short latency to electrical stimulation of the dorsal lateral geniculate nucleus (LGNd) with a burst of three or more spikes at frequencies of 600-900 Hz. These neurons showed a high degree of synaptic convergence, also responding synaptically with a high-frequency burst of spikes to stimulation of both visual area 2 and the corpus callosum.(ABSTRACT TRUNCATED AT 400 WORDS)

Neuronal responses in rabbit cingulate cortex linked to quick-phase eye movements during nystagmus.

1. Responses of single units in area 29 of cingulate cortex were examined in alert rabbits during vestibular and optokinetic nystagmus. Eye movements were measured by optically detecting the position of an infrared light-emitting diode attached to the cornea. 2. Fourteen percent of cingulate cells (68 of 477 isolated units) had responses that were correlated to the occurrence of quick phases. Latencies ranged from 60 ms before to 220 ms after the onset of the quick phase with a mean of 70 ms and standard deviation of 58 ms. Most units responded during or following quick phases, although four units had responses that preceded the quick-phase onset. 3. Unitary responses during quick phases were not due to visual field movement, since these responses occurred in the dark as well as the light. The responses were not dependent upon vestibular stimulation, since responses related to spontaneous saccadelike eye movements were observed in cingulate quick-phase neurons. 4. The majority (37 of 52) of the quick-phase neurons had a directional preference. Approximately equal numbers of directional units responded to quick phases directed ipsilaterally and contralaterally with respect to the recording site. 5. About one-fourth of the quick-phase units were bidirectional (15 of 52) with virtually equal responses to ipsilaterally and contralaterally directed quick phases. 6. Auditory and/or somatosensory responses were observed in only five of the quick-phase cells. All such multimodal units were bidirectional. 7. The quick-phase units were histologically confirmed to be primarily in area 29d of cingulate cortex. Although most cells were located in layer V, some were isolated in layer II-III. 8. Cingulate cortex has reciprocal connections with visual cortex and oculomotor-related thalamic nuclei and projects to the layers of the superior colliculus that are involved in oculomotor control. Responses to quick phases in cingulate neurons may synchronize cingulate cortex responsiveness with the arrival of new, and potentially significant, visual information.

Corticogeniculate neurons, corticotectal neurons, and suspected interneurons in visual cortex of awake rabbits: receptive-field properties, axonal properties, and effects of EEG arousal.

The intrinsic stability of the rabbit eye was exploited to enable receptive-field analysis of antidromically identified corticotectal (CT) neurons (n = 101) and corticogeniculate (CG) neurons (n = 124) in visual area I of awake rabbits. Eye position was monitored to within 1/5 degrees. We also studied the receptive-field properties of neurons synaptically activated via electrical stimulation of the dorsal lateral geniculate nucleus (LGNd). Whereas most CT neurons had either complex (59%) or motion/uniform (15%) receptive fields, we also found CT neurons with simple (9%) and concentric (4%) receptive fields. Most complex CT cells were broadly tuned to both stimulus orientation and velocity, but only 41% of these cells were directionally selective. We could elicit no visual responses from 6% of CT cells, and these cells had significantly lower conduction velocities than visually responsive CT cells. The median spontaneous firing rates for all classes of CT neurons were 4-8 spikes/s. CG neurons had primarily simple (60%) and concentric (9%) receptive fields, and none of these cells had complex receptive fields. CG simple cells were more narrowly tuned to both stimulus orientation and velocity than were complex CT cells, and most (85%) were directionally selective. Axonal conduction velocities of CG neurons (mean = 1.2 m/s) were much lower than those of CT neurons (mean = 6.4 m/s), and CG neurons that were visually unresponsive (23%) had lower axonal conduction velocities than did visually responsive CG neurons. Some visually unresponsive CG neurons (14%) responded with saccadic eye movements. The median spontaneous firing rates for all classes of CG neurons were less than 1 spike/s. All neurons synaptically activated via LGNd stimulation at latencies of less than 2.0 ms had receptive fields that were not orientation selective (89% motion/uniform, 11% concentric), whereas most cells with orientation-selective receptive fields had considerably longer synaptic latencies. Most short-latency motion/uniform neurons responded to electrical stimulation of the LGNd (and visual area II) with a high-frequency burst (500-900 Hz) of three or more spikes. Action potentials of these neurons were of short duration, thresholds of synaptic activation were low, and spontaneous firing rates were the highest seen in rabbit visual cortex. These properties are similar to those reported for interneurons in several regions in mammalian central nervous system. Nonvisual sensory stimuli that resulted in electroencephalographic arousal (hippocampal theta activity) had a profound effect on the visual responses of many visual cortical neurons.(ABSTRACT TRUNCATED AT 400 WORDS)

Thalamic inputs to visual areas 1 and 2 in the rabbit.

Thalamic projections to two cortical representations of the visual field, visual areas 1 and 2 (V1, V2), in the rabbit were studied by using the retrograde transport of horseradish peroxidase (HRP). Physiological guidance was employed to inject small amounts of HRP into topographically defined regions of V1 or V2. Injections restricted to V1 revealed a dense projection from the dorsal lateral geniculate nucleus as well as projections from the pulvinar, the posterior thalamic nucleus, and the ventral lateral nucleus. Injections restricted to V2 revealed projections from the pulvinar, the ventral lateral nucleus, and the posterior thalamic nucleus, but only a slight projection from the dorsal lateral geniculate nucleus. V2, but not V1, receives an input from neurons within the fiber plexus between the dorsal lateral geniculate nucleus and the pulvinar. Finally, the neurons in the lateral geniculate nucleus that project to V2 have larger somata on average than those that project to V1 (means = 18.25 micron vs. 14.04 micron, P less than .001).