Auditory cortical responses to the interactive effects of interaural intensity disparities and frequency.

Under natural conditions, stimuli reaching the two ears contain multiple acoustic components. Rarely does a stimulus containing only one component (e.g. pure tone burst) exist outside the realm of the laboratory. For example, in sound localization the simultaneous presence of multiple cues (spectral content, level, phase, etc.) serves to increase the number of available cues and provide the listener with more information, thereby helping to reduce errors in locating the sound source. The present study was designed to explore the relationship between two acoustic parameters: stimulus frequency and interaural intensity disparities (IIDs). By varying both stimulus frequency and IIDs for each cell, we hoped to gain insight into how multiple cues are processed. To this end, we examined the responses of neurons in cat primary auditory cortex (AI) to determine if their sensitivity to IIDs changed as a function of stimulus frequency. IIDs ranging from +30 to -30 dB were presented at different frequencies (frequency was always the same in the two ears). We found that approximately half of the units examined exhibited responses to IIDs that varied as a function of stimulus frequency (i.e. displayed some form of IID x Freq dependency). The remaining units displayed IID responses that were not clearly related to stimulus frequency.

Positional disparity sensitivity of neurons in the cat accessory optic system.

There is considerable evidence supporting the view that the accessory optic system (AOS) and the closely associated nucleus of the optic tract (NOT) provide visual signals used in the control of optokinetic nystagmus (OKN). In frontal-eyed animals such as the cat and primate, the high degree of overlap in the visual fields of each eye, along with a substantial projection from the visual cortex, gives rise to an increased incidence of binocularly responsive neurons in the AOS. In previous studies, my collaborators and I have shown that visual cortical input to the AOS mediates ipsilateral eye responses and high speed tuning, and can function independently of the contralateral eye. However, beyond fairly gross assessments such as these, the binocular interactions of AOS cells have not been subject to detailed examination. The present study set out to determine whether the responses of binocular cells in the dorsal terminal nucleus (DTN) of the AOS are sensitive to horizontal retinal disparity. Single units were recorded from the DTN of anaesthetized, paralysed cats. A large random-dot pattern was moved under computer control at a constant velocity in the preferred and non-preferred direction. Convergent and divergent disparities were generated by deviating the visual axis of the contralateral (dominant) eye using wedge prisms. The responses of DTN units fell into three categories: (1) cells showing tuned excitatory responses (29% or 7 cells) consisting of a marked facilitation for a single or a limited range of disparities; (2) cells broadly tuned for inhibition (25% or 6 cells); and (3) cells relatively insensitive to disparity (46% or 11 cells), showing a relatively flat response profile across the entire range of disparity conditions, or cells without clear tuning. In summary, this study demonstrates that some AOS cells are sensitive to positional disparity and, therefore, this system may provide signals which specify the plane of motion for ocular stabilization. Some of these results have been presented in brief form [Grasse (1991a) Society of Neuroscience Abstracts, 17, 1380].

Alterations in visual receptive fields in the superior colliculus induced by amphetamine.

Visual response properties were examined in the superficial layers of the superior colliculus (SC) of anesthetized, paralyzed cats before and after i.v. administration of d-amphetamine. Receptive fields (RFs) of single SC units were plotted using small spots of light presented to the contralateral eye. Within the first hour following d-amphetamine injections, RF size gradually increased, reaching a maximum 86 min post-injection. On average, the area of the RF increased by 5.6 times and RF expansion was observed in all single units examined in the superficial layers. Over the subsequent 4-8 h following the injection, RF area gradually decreased and returned to control dimensions. Most RFs displayed asymmetrical patterns of expansion, showing relatively more horizontal than vertical growth. As RF expansion developed, responses to stimuli flashed "on" and "off" at various locations both inside and outside the borders of the control RF became progressively more vigorous. In contrast, no significant changes were noted in direction-selective responses at any time after d-amphetamine injections. Using an array of light bar stimuli of different lengths, the strength of surround suppression was found to be significantly diminished by d-amphetamine. The reduction in surround suppression was especially clear for bar lengths which exceeded the diameter of the control RF. No RF expansion was observed in the superficial layers of the SC when d-amphetamine was injected intravitreally. Furthermore, d-amphetamine had no discernable effect on the RF sizes of cells in the visual cortex. These results suggest that the RF changes in the SC were not of either retinal or cortical origin. We conclude that the mean retinal area which can potentially influence the activity of RFs in the superficial layers of the SC may be on average over 5 times greater than the RF area determined using conventional methods and criteria. These findings raise the interesting possibility that the relatively small size and sharp borders characteristic of RFs in the superficial layers arise from local inhibitory networks which delimit a broader field of excitatory activity supplied by retinal and cortical afferent terminals. Thus, in order to generate the RF changes observed here, either these local inhibitory circuits are amphetamine sensitive, or more likely, these inhibitory networks are dynamically modulated by an, as yet unidentified, amphetamine-sensitive input affecting visual RFs in the superficial layers.

Functional topography of cat primary auditory cortex: responses to frequency-modulated sweeps.

The spatial distribution of neuronal responses to frequency-modulated (FM) sweeps was mapped with microelectrodes in the primary auditory cortex (AI) of barbiturate-anesthetized cats. Increasing and decreasing FM sweeps (upward- and downward-directed FM sweeps, respectively) covering a range of 0.25-64.0 kHz were presented at three different rates of frequency change over time (i.e, sweep speed). Using multiunit recordings, the high-frequency domain (between 3.2 and 26.3 kHz) of AI was mapped over most of its dorsoventral extent (as determined by the distribution of the excitatory bandwidth, Q10dB) for all six cases studied. The spatial distributions of the preferred sweep speed and the preferred sweep direction were determined for each case. Neuronal responses for frequency sweeps of different speeds appeared to be systematically distributed along the dorsoventral axis of AI. In the dorsal region, cortical cells typically responded best to fast and/or medium FM sweeps, followed more ventrally by cells that responded best to medium--then slow--, then medium-speed FM sweeps. In the more ventral aspect of AI (which in some cases may also have included cells located in the dorsal region of the second auditory field, AII), neurons generally preferred fast FM sweeps. However, a comparison of maps from different animals showed that there was more variability in the distribution of preferred speed responses in the ventral region of the cortex. The directional preference of units for FM sweeps was determined for the sweep speed producing the strongest response. Direction selectivity appeared to be nonrandomly distributed along the dorsoventral axis of AI. In general, units that responded best to upward-directed FM sweeps were located in the more dorsal and ventral aspects of AI while units that responded best to downward-directed FM sweeps were usually located in the mid-region of AI. Direction selectivity was also determined for multiunit responses at each of the three FM sweep speeds. In general, there was a relatively close agreement between the spatial distributions of direction selectivity determined for the strongest response with those calculated for the fast and medium speeds. The spatial distribution of direction selectivity determined for slow FM sweeps deviated somewhat from that determined for the strongest response. Near the dorsoventral center of the mapped areas, the distribution of units that responded best to downward sweeps tended to overlay the distribution of units that responded best to slow speeds, suggesting some spatial covariance of the two parameters.(ABSTRACT TRUNCATED AT 400 WORDS)

A comparison of monaural and binaural responses to frequency modulated (FM) sweeps in cat primary auditory cortex.

Monaural and binaural single unit responses to frequency-modulated (FM) sweeps were compared in cat primary auditory cortex (AI). Both upward-directed (changing from low to high frequency) and downward-directed (changing from high to low frequency) FM sweeps were presented monaurally and binaurally at five rates of frequency modulation (referred to here as the speed of FM sweep). Two types of binaural FM sweep conditions were presented: (1) like-directed FM sweeps, in which identical FM sweeps were presented to both ears, and (2) opposite-directed FM sweeps, in which one ear was presented with one direction of FM sweep while the other ear was simultaneously presented with the opposite direction of FM sweep. In a sample of 78 cells, 33 cells were classified as EE (binaural facilitatory) and 45 were classified as EI (binaural inhibitory). Ninety-four percent of all units were sensitive to the direction and/or speed of FM sweeps. In general, under binaural stimulus conditions, EE cells responded optimally to like-directed FM sweeps, while EI cells preferred opposite-directed FM sweeps. When tested monaurally, 59% of all cells (both EE and EI) were direction selective, with the majority (76%) preferring downward-directed FM sweeps. When tested binaurally, most direction selective EE cells (60%) preferred upward-directed FM sweeps, while the majority of direction selective EI cells (71%) preferred downward-directed FM sweeps. Our analysis also allowed us to classify inhibitory responses of EI cells as either direction selective (37%) or non-direction selective (63%). For FM speed selectivity under monaural conditions, most EE cells preferred fast FM sweep rates (0.4-0.8 kHz/ms), while approximately equal numbers of EI cells preferred either slow (i.e., 0.05-0.1 kHz/ms) or fast (i.e., 0.4-0.8 kHz/ms) speeds. Under binaural conditions, the majority of EE and EI cells responded best to high speeds when tested with like-directed FM sweeps, while the preferred speed with opposite-directed FM sweeps was more broadly tuned. The results suggest the presence of binaural neural mechanisms underlying cortical FM sweep direction and speed selectivity.

Analysis of a naturally occurring asymmetry in vertical smooth pursuit eye movements in a monkey.

1. We have investigated the mechanism of a directional deficit in vertical pursuit eye movements in a monkey that was unable to match upward eye speed to target speed but that had pursuit within the normal range for downward or horizontal target motion. Except for a difference in the axis of deficient pursuit, the symptoms in this monkey were similar to those seen with lesions in the frontal or parietal lobes of the cerebral cortex in humans or monkeys. Our evaluation of vertical pursuit in this monkey suggests a new interpretation for the role of the frontal and parietal lobes in pursuit. 2. The up/down asymmetry was most pronounced for target motion at speeds greater than or equal to 2 degree/s. For target motion at 15 or 30 degree/s, upward step-ramp target motion evoked a brief upward smooth eye acceleration, followed by tracking that consisted largely of saccades. Downward step-ramp target motion evoked a prolonged smooth eye acceleration, followed by smooth, accurate tracking. 3. Varying the amplitude of the target step revealed that the deficit was similar for targets moving across all locations of the visual field. Eye acceleration in the interval 0-20 ms after the onset of pursuit was independent of initial target position and was symmetrical for upward and downward target motion. Eye acceleration in the interval 60-80 ms after the onset of pursuit showed a large asymmetry. For upward target motion, eye acceleration in this interval was small and did not depend on initial target position. For downward target motion, eye acceleration depended strongly on initial target position and was large when the target started close to the position of fixation. 4. We next attempted to understand the mechanism of the up/down asymmetry by evaluating the monkey's vertical motion processing and vertical eye movements under a variety of tracking conditions. For spot targets, the response to upward image motion was similar to that in normal monkeys if the image motion was presented during downward pursuit. In addition, the monkey with deficient upward pursuit was able to use upward image motion to make accurate saccades to moving targets. We conclude that the visual processing of upward image motion was normal in this monkey and that an asymmetry in visual motion processing could not account for the deficit in his upward pursuit. 5. Upward smooth eye acceleration was normal when the spot target was moved together with a large textured pattern.(ABSTRACT TRUNCATED AT 400 WORDS)

Pharmacological isolation of visual cortical input to the cat accessory optic system: effects of intravitreal tetrodotoxin on DTN unit responses.

Direction-selective responses were recorded from neurons in the dorsal terminal nucleus (DTN) of the cat accessory optic system before and after intravitreal injections of tetrodotoxin (TTX) into the contralateral eye. After approximately 100 min, direction-selective responses driven through stimulation of the contralateral, injected eye were reduced on average by 90%, while direction-selective responses driven through stimulation of the ipsilateral, uninjected eye were not significantly reduced. By 200 min postinjection, ipsilateral direction-selective responses were either equal to or sometimes greater than control values. In the final stages of these experiments (i.e. between 390-830 min after contralateral eye injections), ipsilateral eye responses were on average 30% higher than control. The effects of retinal blockade of the contralateral eye by TTX show that input from the ipsilateral eye alone is sufficient to mediate direction-selective responses in DTN cells. These results and those observed following bicuculline eye injections reported previously (Grasse et al. 1990) demonstrate that direction-selective responses in the DTN driven through stimulation of the contralateral and ipsilateral eyes arise from independent neural mechanisms located in the retina and visual cortex, respectively. Moreover, these findings also suggest that the contralateral eye exerts an inhibitory influence over ipsilateral eye responses which is diminished by TTX injections into the contralateral eye.

Direction-selective responses of units in the dorsal terminal nucleus of cat following intravitreal injections of bicuculline.

Extracellular recordings from single units in the dorsal terminal nucleus (DTN) of the cat accessory optic system (AOS) were made before and after intravitreal injections of the GABA antagonist bicuculline methiodide (BMI). Direction-selective responses of DTN cells elicited through the contralateral, injected eye were abolished 7-12 h following the injection. For the concentrations tested, direction-selective responses through the contralateral (injected) eye did not recover within 26 h. Direction-selective responses through stimulation of the ipsilateral (uninjected) eye were also dramatically depressed for 1-9 h after contralateral eye injections. However, direction-selective responses through the ipsilateral eye eventually returned and were often more vigorous in the final stages. BMI injections into the ipsilateral eye failed to block direction-selective responses through the ipsilateral eye. The effects of intravitreal BMI on contralateral eye responses imply that DTN units receive input from direction-selective retinal ganglion cells. In addition, these results suggest that direction-selective input to the DTN from the visual cortex is independent of the retinal pathway. Using pharmacological methods described here, for the first time direction-selective responses of AOS units driven through the ipsilateral eye can be experimentally isolated.

The effect of visual cortex lesions on vertical optokinetic nystagmus in the cat.

Vertical optokinetic nystagmus (VOKN) was measured before and after visual cortex lesions using the magnetic search coil technique. In normal cats, upward motion elicits higher slow phase gain than downward motion, especially at high stimulus velocities. Following decortication, the gain of upward VOKN may be attenuated by as much as 35% at stimulus velocities of 20% or more. This high velocity deficit in upward VOKN is consistent with the results of single unit studies of the lateral terminal nucleus (LTN) of the accessory optic system which suggest that visual cortical input (via the LTN) makes a direction specific contribution to the motion sensitivity of VOKN.

The accessory optic system of the monocularly deprived cat.

Single-unit extracellular recordings were made in the lateral (LTN) and dorsal (DTN) terminal nuclei of the accessory optic system (AOS) of 10 monocularly deprived cats. The separate effects of monocular deprivation (MD) observed in each hemisphere are outlined below. Unlike many units in normal animals, LTN and DTN cells in the hemisphere contralateral to the non-deprived (open) eye, were no longer activated through visual stimulation of the ipsilateral (deprived) eye. In both nuclei, cells were driven effectively only by stimuli presented via the contralateral eye. The distribution of preferred directions was considerably altered in the LTN but not in the DTN. Almost every LTN unit encountered in MD cats preferred downward stimulus motion, in contrast to normal animals where equal numbers of LTN cells show preferences for upward and downward movement (J. Neurophysiol., 51 (1984) 276-293). DTN units showed the usual preference for horizontal motion toward the recorded hemisphere. Velocity preferences were slower on average in the DTN, and unaffected in the LTN. In the hemisphere contralateral to the deprived eye, the ocular dominance distribution of LTN and DTN cells showed a distinct shift in favor of the contralateral (deprived) eye. This effect was not as complete as that observed in the other hemisphere. Cells in both nuclei displayed a small influence from the ipsilateral (exposed) eye in some animals, but this input was much less than that observed in normally reared cats. Average velocity preferences among DTN units were slower than normal, and slower relative to the DTN population in the opposite hemisphere. No pronounced changes were observed in LTN velocity tuning. The distributions of preferred directions for both nuclei were similar to those obtained in the other hemisphere: DTN cells were found to prefer horizontal motion, while most LTN units were activated best by stimuli moving vertically and down within their receptive fields.

Response properties of single units in the accessory optic system of the dark-reared cat.

The visual responses of single units in the lateral and dorsal terminal nuclei (LTN and DTN) of the accessory optic system (AOS) were studied in adult cats reared in total darkness. In the LTN of the normal cat equal numbers of cells prefer upward and downward vertical stimulus motion (previous results). While direction selectively continued to be a characteristic property of LTN and DTN units in dark-reared animals, the distribution of preferred and non-preferred directions of LTN cells was radically altered such that almost every LTN cell examined in the dark-reared cat preferred downward stimulus motion. In contrast, the distribution of preferred directions among DTN cells was largely unaffected by dark rearing. Both normal and dark-reared cat DTN cells responded best to stimuli moving horizontally toward the recorded hemisphere. The velocity preferences of DTN units of the dark-reared cat were, however, much slower than those of normal DTN units. LTN units responding to downward motion in dark-reared cats showed similar velocity preferences to those downward direction-selective LTN units in normal animals. Unlike the highly binocular responses of AOS cells encountered in the normal cat, the ocular dominance distribution obtained from units in the LTN and DTN of the dark-reared cat is completely monocular, favoring the contralateral eye. Thus, dark rearing renders the distribution of preferred directions most affected in the LTN, velocity preference most affected in the DTN and ocular dominance strongly affected in both nuclei. The physiological response properties of the dark-reared cat presented in this report bear a close resemblance to those we have described in the AOS of acutely decorticated animals (previous results). Data obtained from the dark-reared cat support our earlier suggestion that the visual cortex is a major source of upward direction selectively, high-velocity tuning and ipsilateral eye input for AOS cells. Some of the functional consequences of these findings are discussed in relation to frontal eye placement and optokinetic nystagmus.

Basal optic complex in the frog (Rana pipiens): a physiological and HRP study.

The basal optic projection in the frog Rana pipiens has been investigated by single-unit extracellular recording and horseradish peroxidase (HRP) histochemistry. We approached the projection from the ventral side of the brain and recorded single units in the basal optic projection proper as well as in the adjacent dorsomedial region (jointly called the basal optic complex). We found a) units responsive to stimuli moving in a vertical direction, b) an approximately equal number of units responsive to stimuli moving in a horizontal direction, and c) a smaller number of units responsive to changes in ambient light and moving stimuli without direction selectivity. Directional units display significant maintained activity and usually decrease their firing rate in response to stimulus motion in a direction opposite to that which elicits the maximal increase in firing rate. Receptive-field sizes for directional units ranged from 10 to 60 degrees. All units displayed vigorous excitatory response to a wide variety of moving stimuli within the velocity range of 0.2-10 degree/s. HRP histochemistry shows that in addition to the retina, the basal optic complex is connected to three principal areas: the ipsilateral tegmental griseum centrale, the ipsilateral dorsal ventrolateral nucleus of the anterior thalamus, and the ipsilateral posterior thalamic nucleus. In addition, a pathway was observed consisting of two groups of cells that send axons to the ipsilateral rostroventral medulla. This pathway originates a) in cells whose somata lie within the dorsomedial aspect of the basal optic complex (BOC); and b) in cells whose somata lie immediately outside the BOC in the adjacent gray, with apical dendrites extending into the BOC. Some of these fibers continue to the level of the spinal cord. Injection of HRP into the rostroventral medulla led to retrograde labeling of cells of the BOC.

Electrophysiology of lateral and dorsal terminal nuclei of the cat accessory optic system.

Visual responses were examined quantitatively in 96 units in the lateral (LTN) and dorsal (DTN) terminal nuclei of the cat accessory optic system (AOS). The receptive fields of LTN and DTN cells were quite large, with an average diameter of approximately 60 degrees. Individual cell receptive fields, which could be as small as 30 degrees vertically by 15 degrees horizontally or as large as 100 by 100 degrees, always included the area centralis. Large, moving textured stimuli provoked optimal modulation in these cells. In response to a 100 by 80 degrees random-dot pattern moving at a constant velocity, nearly all cells in both the LTN and DTN displayed a high degree of direction selectivity. Directional response profiles were subjected to a vector analysis that generated two quantities proportional to the direction and magnitude of the major excitatory (E vectors) and inhibitory (I vectors) responses of individual cells. Directional vectors of the LTN displayed a strikingly bimodal distribution: E vectors of individual LTN cells pointed either upward (25 of 49) or downward (23 of 49). I vectors also pointed either up or down in a direction opposite to that of the E vector for the same cell. E and I vectors in both LTN and DTN units were separated by approximately 180 degrees. With few exceptions, E vectors of DTN cells pointed in a horizontal-medial direction, while DTN I vectors pointed in a horizontal-lateral direction. A relatively broad range of stimulus velocities (0.8-102.4 degrees/s) evoked maximal excitation in individual LTN units. The majority of LTN cells, however, achieved maximal excitation at velocities between 0.8 and 12.8 degrees/s. The deepest inhibition was elicited over a range of velocities from 0.2 to 102.4 degrees/s, with two major peaks at 0.8 and 12.8 degrees/s. A similar range of velocity sensitivity was observed in DTN cells: maximal excitation was obtained for stimulus velocities from 1.6 to 102.4 degrees/s, with most DTN cells showing the greatest excitatory response between 6.4 and 12.8 degrees/s. A broad range of inhibitory velocity tuning was also observed in DTN units, with most cells exhibiting the deepest inhibitory modulation at 25.6 degrees/s. The majority of LTN and DTN units were driven most effectively through the eye contralateral to the recording site. Nonetheless, a large percentage of LTN (78%) and DTN (93%) cells could be driven to some extent through both eyes. Despite this conspicuous ipsilateral eye influence, no units were found in either the LTN or the DTN that were driven solely through the ipsilateral eye.(ABSTRACT TRUNCATED AT 400 WORDS)

Alterations in response properties in the lateral and dorsal terminal nuclei of the cat accessory optic system following visual cortex lesions.

The response properties of cells in the lateral (LTN) and dorsal (DTN) terminal nuclei of the accessory optic system (AOS) were examined in 14 cats which underwent unilateral visual cortex ablation. Following decortication, single units in the LTN and DTN no longer showed the high degree of binocular convergence characteristic of the intact animal, but instead LTN and DTN units became almost completely dominated by the contralateral eye. In addition, responsivity of LTN and DTN cells to high stimulus velocities was abolished by removal of cortical input. This decrement in high velocity response was observed in both the excitatory and the inhibitory components of the velocity response profile. While the incidence of direction selective neurons in both the LTN or the DTN was not affected by decortication, the distribution of preferred and nonpreferred directions was dramatically altered in the LTN, and to a lesser extent in the DTN. In the LTN, there was a severe reduction in the number of cells which displayed maximal excitation for upward stimulus motion. Instead, most LTN units in the decorticate cat preferred downward directed stimulus motion. In the DTN, most units still preferred horizontal stimulus motion as in the intact animal, but the overall distribution of preferred directions displayed a clear downward vertical vector component. In other respects, such as receptive field size and position in visual space, on/off responses, and resting discharge rate, LTN and DTN units appeared unaffected by cortical lesions. These experiments demonstrate that the cortical input to the LTN and DTN plays a highly significant role in the formation of response properties of cells located in these nuclei. The results presented in this report indicate that the visual cortex is a major source of ipsilateral eye input, high velocity responses, and upward direction selectivity for the AOS units examined in these experiments.

Retinal degeneration in cats fed casein. IV. The early receptor potential.

Electroretinographic studies of casein-fed cats with retinal taurine deficiency revealed that the early receptor potential (ERP) was initially normal in amplitude at a time when the a-wave and b-wave of the electroretinogram were substantially reduced or even nondetectable. The preserved ERP's in these taurine-deficient cats could be correlated with the histologic finding that their outer segments were relatively intact over 90% of the retinal area subtended by the test flash. The sequence of electroretinographic changes in these taurine-deficient cats was also consistent with previous biochemical studies on the normal cat retina that have shown a relatively low concentration of taurine at the level of the outer segments and a higher concentration at the level of the inner segments. The responses in early stages from taurine-deficient cats differed from the responses obtained from vitamin A--deficient cats but resembled those from cats that received an intravitreal injection of ouabain. Similarities and a difference between the responses of taurine-deficient cats and those of patients with early retinitis pigmentosa are considered.