Functionally distinct groups of X-cells in the lateral geniculate nucleus of the cat.

The latencies and visual response properties of 202 X-cells in the A-laminae of the cat dorsal lateral geniculate nucleus (LGN) were examined to investigate the recent claim (Mastronarde, '85,'87a) that functionally different groups of X-cells reside there. Two groups of X-cells were found, which differed in their extracellularly recorded responses to spots of light flashed within their receptive fields. One group, constituting one-third of the sample, responded to spot onset with a profound and often long-lasting dip in discharge rate, such that cell discharge usually did not reach half maximum until greater than or equal to 100 msec after spot onset. About 70% of these cells also displayed a transient discharge at spot onset. These cells correspond to Mastronarde's lagged X-cells, and we similarly refer to them as XL-cells. The second group, constituting the remainder of the X-cell population, generally responded to spot onset with a short latency (less than or equal to 60 msec) brisk discharge, no detectable XL-type dip, and a rapid reduction in firing at spot offset. We refer to these neurons as nonlagged (XN) X-cells; this group probably encompasses all of Mastronarde's non-XL-cells. Despite some overlap, the XL- and XN-cells differed in numerous other features. Compared to XN-cells, XL-cells exhibited: 1) lower peak rates of discharge and more uniform firing during spot onset; 2) slightly longer latencies and markedly lower probabilities of discharge to optic chiasm stimulation; 3) consistently lower geniculocortical conduction velocities; and 4) markedly lower optimal temporal frequencies when tested with drifting sine wave gratings. No differences were found between the two cell groups in optimal spatial frequency, spatial resolution, or receptive field center size, and there were equal proportions of on- and off-center types of XL- and XN-cells. Analyses of one- and two-dimensional plots of the physiological measures indicate that XL- and XN-cells constitute a physiological continuum. However, the two groups occupy opposite sides of the continuum on many of the measures, with little overlap and with few (less than 5%) cells with intermediate properties. Therefore, XL-cells may be considered a distinct, readily identifiable group. These findings confirm and extend Mastronarde's ('87a) observations on functional differences among geniculate X-cells.(ABSTRACT TRUNCATED AT 400 WORDS)

Structural correlates of functionally distinct X-cells in the lateral geniculate nucleus of the cat.

In the companion paper (Humphrey and Weller, '88), we demonstrated 2 physiologically different groups of X-cells (XL and XN) in the A-laminae of the cat lateral geniculate nucleus. In order to investigate their possible morphological correlates, we iontophoresed horseradish peroxidase intracellularly into physiologically identified XL- and XN-cells and examined their light microscopic appearance. The 11 HRP-labeled XL-cells constituted the smallest relay neurons in the A-laminae, and were similar morphologically. All had small somata (mean soma size = 236 micron2), very thin (less than 1.0 micron) axons, few primary dendrites, and narrow, sinuous distal dendrites, which usually formed trees that were oriented perpendicular to laminar borders. The dendrites could be smooth or display beadlike varicosities, hairlike appendages, and/or occasional complex stalked appendages, but their most consistent feature was numerous clusters of grapelike dendritic appendages located at or near dendritic branch points. The 14 labeled XN-cells were structurally more heterogeneous, and they included relay neurons and interneurons. Eight of 11 XN-relay cells differed markedly from the XL-cells. These XN-cells were multipolar neurons with medium to large somata (mean soma size = 365 micron2), small to medium-size axons (1.0-2.0 micron), numerous primary dendrites, and straight distal dendrites that formed radially symmetric trees. The dendrites of the cells were largely smooth, except for occasional spines and/or hairs, and they were devoid of grapelike and other complex appendages. The three other XN-relay neurons had morphologies either similar to XL-cells or intermediate between XL-cells and more simple, multipolar XN-relay cells, but two of these cells had larger somata and axons than most XL-cells. Finally, three XN-cells were intrageniculate interneurons, which possessed small somata (mean soma size = 174 micron2), fine sinuous dendrites covered with beadlike varicosities on stalked appendages, and no obvious axon. These results reveal that, despite minor overlap, there are marked structural differences between XL- and XN-cells. Among the relay cells, these differences relate to soma and axon diameter, dendritic orientation, and the presence or absence of grapelike dendritic appendages. Our finding that interneurons were strongly excited at short latencies by spot onset supports the hypothesis (Mastronarde, '87a; Humphrey and Weller, '88) that such interneurons provide the major inhibitory input to XL-cells, and that this input is important in generating the spot-induced early dips in XL-cell discharge.

Topographic organization of the orientation column system in the striate cortex of the tree shrew (Tupaia glis). I. Microelectrode recording.

Microelectrode recordings were made in the binocular portion of the tree shrew striate cortex to determine how orientation selective cells are distributed topographically in area 17 of this species. Seventy-five percent of the cells sampled were activated well by elongated visual stimuli and were quite selective for stimulus orientation. Ninety-five percent of the orientation-selective cells had orientation tuning ranges (Wilson and Sherman, '76) between +/- 5 degrees and +/- 40 degrees from their optimal orientation. Orientation-selective cells with the same or similar optimal orientations were distributed in cortex in a columnar manner (Hubel and Wiesel, '62), as determined from electrode penetrations nearly normal to the cortical surface. Penetrations parallel to the cortical surface revealed a highly ordered representation of optimal stimulus orientation, generally characterized by sequential changes in optimal orientation with electrode movement across the striate cortex. In addition, relatively consistent differences were observed in the rates and patterns of orientation shift on these penetrations depending on the direction of electrode movement across the cortex. Penetrations parallel to the 17--18 border yielded moderate-to-high rates of orientation change (mean slope = 434 degrees/mm), with the changes generally progressing through a complete clockwise or counterclockwise cycle of 180 degrees or more before a major reversal in the direction of orientation shift was encountered. In contrast, penetrations perpendicular to the border yielded low-to-moderate slopes (mean slope = 239 degrees/mm). On these penetrations a more limited range of optimal orientations (< 180 degrees) was usually encountered, due to frequent reversals in the direction of orientation shift. Also, extended regions (100--200) micrometers long) of constant optimal orientation were observed in these penetrations. The different patterns of orientation change found on these orthogonal penetrations across the striate cortex indicate that the orientation column system in this species is anisotropically organized with respect to the 17--18 border. Further, the regions of constant optimal orientation frequently encountered on penetrations perpendicular to the 17--18 border suggest that the anisotropy is subserved by a system of elongated zones of iso-orientation arranged approximately perpendicular to the 17--18 border.

Projection patterns of individual X- and Y-cell axons from the lateral geniculate nucleus to cortical area 17 in the cat.

Horseradish peroxidase was injected intracellularly into single, physiologically-identified X- and Y-cell geniculocortical axons projecting to area 17 of the cat. This injection anterogradely labeled the axon terminal fields in cortex and retrogradely labeled the somata of these same axons in laminae A and A1 of the lateral geniculate nucleus (LGN). The laminar projections of 21 X- and 15 Y-cell axons were analyzed. For these, the laminar terminations of ten X- and seven Y-cell axons were also related to their cells' positions in the A-laminae. The terminal fields of X- and Y-cell axons overlapped substantially in layers IV and VI of area 17. Some X-cells terminated mainly in IVb, others mainly in IVa, and still others throughout IVa and IVb. The latter two groups also projected up to 100 micron into lower layer III. Y-cells terminated primarily in layer IVa and projected up to 200 microns into lower layer III. Some also arborized throughout the depth of layer IVb. Both X- and Y-cell axons terminated throughout the depth of layer VI, although more so in the upper half. We found no relationship between the diameter of the parent axon and its sublaminar projection within layer IV. Within layer IV, X-cell axons generally terminated within a single, continuous clump and had surface areas of 0.6 to 0.9 mm2. Axons of Y-cells often terminated in two to three separate clumps, separated by terminal free gaps 400 to 600 micron wide. Their total surface areas, including gaps, were 1.0 to 1.8 mm2, roughly 1.6 times the surface areas of X-cell axons. Despite considerable overlap, Y-cell arbors contained significantly more boutons than did X-cell arbors. The sublaminar projections of the X- and Y-cell axons within layer IV reflected the locations of the cells' somata within the depth of the A-laminae. X-cells located in the dorsal or ventral thirds of the depths of the laminae projected mainly to layer IVa or throughout layer IV in cortex. Those located in the central thirds projected mainly to layer IVb. Y-cells showed a similar positional relationship, but they appeared to follow different rules. Y-cells in the outer thirds of the A-laminae projected mainly to layer IVa; those in the central thirds, in addition, expanded their projections to include layer IVb. In general, larger sized somata in the LGN gave rise to more widely spreading terminal arbors and greater numbers of boutons in cortex than did smaller somata.(ABSTRACT TRUNCATED AT 400 WORDS)

Termination patterns of individual X- and Y-cell axons in the visual cortex of the cat: projections to area 18, to the 17/18 border region, and to both areas 17 and 18.

Horseradish peroxidase was injected intracellularly into single, physiologically identified X- and Y-cell geniculocortical axons that projected to area 18, to the 17/18 border region, or to both areas 17 and 18 via branching axons. The axon terminal fields in cortex were labeled anterogradely, and the cell bodies of the axons in the A-laminae, lamina C, and the medial interlaminar nucleus (MIN) of the dorsal lateral geniculate nucleus (LGN) were labeled retrogradely. The laminar projections in area 18 of eight Y-cells and one geniculate, non-Y-cell were analyzed. Most of the cells arborized densely within layer IVa and the lower 200 to 400 microns of layer III. Most provided little or no input to layer IVb or layer VI. Thus, the laminar projections of Y-cells to layer IV of area 18 were similar to those of their area 17 counterparts, although the input to layer III was greater and rose much higher in area 18 than in area 17. The terminal arbors in area 18 were two to three times larger in lateral extent than those in area 17. They spread over 2.0 to 2.8 mm2 of layer IV and occupied proportionately much greater regions of area 18 than the Y-cell arbors in area 17. This may partially account for the large receptive fields of cortical cells in area 18, and it indicates that a small region of area 18 may receive converging inputs from a relatively wide retinotopic region of the LGN. The terminal arbors were also highly asymmetric, generally being two to four times longer anteroposteriorly than mediolaterally. These asymmetric arbors may form the structural basis for the anisotropic organization of the retinotopic map in area 18. We recovered three cells (two Y, one X) whose axons arborized in the border zone between areas 17 and 18. One Y-cell axon had a receptive field located in the ipsilateral visual hemifield and it arborized in a small region restricted almost exclusively to the border zone. The other two cells had receptive fields on or adjacent to the vertical meridian, and they terminated on either side of the 17/18 border region as well as within it. Thus, geniculate afferents representing the ipsilateral hemifield or the vertical meridian appear to have different patterns of termination on and adjacent to the 17/18 border zone. Also, some X-cell input may invade area 18 in the region immediately adjacent to the border zone.(ABSTRACT TRUNCATED AT 400 WORDS)

Anatomical binding of intrinsic connections in striate cortex of tree shrews (Tupaia glis).

The intrinsic connectivity of striate cortex was investigated by injecting horseradish peroxidase (HRP) into this area in tree shrews. Such HRP injections demonstrated periodically organized, stripelike connections within area 17. These stripes occur in layers I-IIIA and consist of a small number or retrogradely filled neurons, some clearly pyramidal, together with HRP-labeled axon terminals. HRP-filled axons trunks run between labeled stripes, interconnecting adjacent and distant regions of the stripe pattern. Correlation with Golgi-stained tissue suggests that these stripes are horizontally interconnected by pyramidal neurons with long intracortical axon collaterals (followed for distances over 1 mm from the soma). The HRP-labeled strips measure about 230 micrometers in width, with a center-to-center repeat distance of 450--500 micrometers. They have been mapped over an 8 mm2 area of striate cortex and would thus seem capable of effecting lateral interactions over considerable portions of the retinotopic map. In their dimensions and overall pattern, these anatomical stripes resemble the 2-deoxyglucose (2-DG) bands resulting from visual stimulation of trees shrews with stripes of a single orientation. While the functional role of the HRP-labeled stripes is unclear, their similarities with the 2-DG pattern raise the intriguing possibility that they may be related to orientation selectivity. The striking regularity of these extensive lateral interconnections emphasizes the importance of horizontal intralaminar connections within the cortex.

Topographic organization of the orientation column system in the striate cortex of the tree shrew (Tupaia glis). II. Deoxyglucose mapping.

The topographic organization of the orientation column system in the tree shrew striate cortex was examined by using 2-deoxyglucose autoradiography to map the cortical sites of increased metabolic activity produced by visual stimulation with stripes of a single orientation. Awake experimental tree shrews (freely moving, restrained, or paralyzed) were given injections of deoxyglucose label and then stimulated with vertical, horizontal, or oblique stripes for 45--75 min. Autoradiographs of coronal sections through the striate cortex revealed regularly spaced radial zones of increased deoxyglucose uptake 150--350 micrometers wide, extending from the cortical surface to the white matter, separated by interzone regions of lower uptake. The radial zones were most densely labeled and distinct in layers I--IIIb and least distinct in layer IV, which was continuously and densely labeled throughout both the radial zone and interzone regions. These radial zones, which were not present in control animals that viewed many orientations, reflect the locations of cortical cells activated by a single stimulus orientation. Reconstructions of the radial zones from serial sections produced maps of the distribution of increased deoxyglucose uptake across striate cortex. The maps reveal a highly organized system of narrow, parallel bands that are slightly wavy and have a mean spacing of 530 micrometers. The band pattern was confirmed in sections cut tangential to the cortical surface and was similar in animals stimulated with either vertical or horizontal stripes; the bands consistently abut the 17--18 border at nearly right angles and extend across the striate cortex in a generally posteromedial direction. These patterns of increased deoxyglucose consumption confirm the anisotropic distribution of orientation-selective cells across the tree shrew striate cortex, suggested in the preceding microelectrode study (Humphrey and Norton, '80). The density distribution of label within the bands further suggests that the anisotropy is due to a system of parallel, somewhat wavy iso-orientation lines arranged roughly perpendicular to the 17--18 border.

Action of brain stem reticular afferents on lagged and nonlagged cells in the cat lateral geniculate nucleus.

1. The A-laminae of the cat lateral geniculate nucleus (LGN) contain two distinct groups of relay neurons: lagged and nonlagged cells. The groups differ in the pattern, timing, and amplitude of response to flashing spots. At spot onset, nonlagged cells discharge at short latency with an excitatory transient; in lagged cells this transient is supplanted by an inhibitory dip and a delayed latency to discharge. At spot offset, lagged cell discharge decays more slowly than in nonlagged cells. Here we have investigated the facilitatory influence of the brain stem reticular formation on the response properties of lagged X-cells (XL) and nonlagged X- and Y-cells (XN and YN). We were particularly interested in whether the inhibitory dip and sluggish response of lagged cells could be reversed during brain stem activation and the cells induced to respond like nonlagged cells. The peribrachial region (PB) of the pontine reticular formation was stimulated electrically with the use of 1,100-ms-long pulse trains that were paired with flashing spot stimuli. 2. Stimulation of PB led to an increase in the amplitude of visually evoked discharge in lagged and nonlagged cells. Compared with their response to spot stimulation alone, the average PB-evoked increase in mean discharge rate was greater than 50% in both groups. The mean discharge rate during PB plus spot stimulation was somewhat higher for XN-cells than for YN- and XL-cells, reflecting the relatively higher discharge rate among XN-cells during spot stimulation alone. 3. Two measures of response timing characterize lagged and nonlagged cells: latency to half-maximal discharge at spot onset (half rise) and latency to half-minimal discharge at spot offset (half fall). Among XN- and YN-cells, PB stimulation had no significant effect on these two latencies; among XL-cells, both latencies were reduced by 43 and 35%, respectively, on average. 4. During spot stimulation alone, all lagged cells were distinguishable from all nonlagged cells in having half-rise and half-fall latencies greater than 60 ms. Despite the reduction among XL-cells in these 2 latencies during PB stimulation, all but 2 of the 40 XL-cells maintained laggedlike latencies. The majority (95%) of XL-cells remained unambiguously lagged on these measures during brain stem stimulation. 5. During spot stimulation alone, 30 of 40 XL-cells tested displayed a prominent and often long-lasting inhibitory dip in discharge starting approximately 45 ms after spot onset. During PB stimulation only three cells lost the dip.(ABSTRACT TRUNCATED AT 400 WORDS)

Evidence of input from lagged cells in the lateral geniculate nucleus to simple cells in cortical area 17 of the cat.

1. The visual cortex receives several types of afferents from the lateral geniculate nucleus (LGN) of the thalamus. In the cat, previous work studied the ON/OFF and X/Y distinctions, investigating their convergence and segregation in cortex. Here we pursue the lagged/nonlagged dichotomy as it applies to simple cells in area 17. Lagged and nonlagged cells in the A-layers of the LGN can be distinguished by the timing of their responses to sinusoidally luminance-modulated stimuli. We therefore used similar stimuli in cortex to search for signs of lagged and nonlagged inputs to cortical cells. 2. Line-weighting functions were obtained from 37 simple cells. A bar was presented at a series of positions across the receptive field, with the luminance of the bar modulated sinusoidally at a series of temporal frequencies. First harmonic response amplitude and phase values for each position were plotted as a function of temporal frequency. Linear regression on the phase versus temporal frequency data provided estimates of latency (slope) and absolute phase (intercept) for each receptive-field position tested. These two parameters were previously shown to distinguish between lagged and nonlagged LGN cells. Lagged cells generally have latencies > 100 ms and absolute phase lags; nonlagged cells have latencies < 100 ms and absolute phase leads. With the use of these criteria, we classified responses at discrete positions inside cortical receptive fields as lagged-like and nonlagged-like. 3. Both lagged-like and nonlagged-like responses were observed. The majority of cortical cells had only or nearly only nonlagged-like zones. In 15 of the 37 cells, however, the receptive field consisted of > or = 20% lagged-like zones. For eight of these cells, lagged-like responses predominated. 4. The distribution of latency and absolute phase across the sample of cortical simple cell receptive fields resembled the distribution for LGN cells. The resemblance was especially striking when only cells in or adjacent to geniculate recipient layers were considered. Absolute phase lags were almost uniformly associated with long latencies. Absolute phase leads were generally associated with short latencies, although cortical cells responded with long latencies and absolute phase leads slightly more often than LGN cells. 5. Cells in which a high percentage of lagged-like responses were observed had a restricted laminar localization, with all but two being found in layer 4B or 5A. Cells with predominantly nonlagged-like responses were found in all layers. 6. Lagged-like zones can not be easily explained as a result of stimulating combinations of nonlagged inputs.(ABSTRACT TRUNCATED AT 400 WORDS)

Spatial and temporal response properties of lagged and nonlagged cells in cat lateral geniculate nucleus.

1. It has recently been shown that the X- and Y-cell classes in the A-layers of the cat lateral geniculate nucleus (LGN) are divisible into lagged and nonlagged types. We have characterized the visual response properties of 153 cells in the A-layers to 1) reveal response features that are relevant to the X/Y and lagged/nonlagged classification schemes, and 2) provide a systematic description of the properties of lagged and nonlagged cells as a basis for understanding mechanisms that affect these two groups. Responses to flashing spots and drifting gratings were measured as the contrast and spatial and temporal modulation were varied. 2. X- and Y-cells were readily distinguished by their spatial tuning. Y-cells had much lower preferred spatial frequencies and spatial resolution than X-cells. Within each functional class (X or Y), however, lagged and nonlagged cells were similar in their spatial response properties. Thus the lagged/nonlagged distinction is not one related to the spatial domain. 3. In the temporal domain X- and Y-cells showed little difference in temporal tuning, whereas lagged and nonlagged cells showed distinctive response properties. The temporal tuning functions of lagged cells were slightly shifted toward lower frequencies with optimal temporal frequencies of lagged X-cells averaging an octave lower than those of nonlagged X-cells. Temporal resolution was much lower in lagged X- and Y-cells than in their nonlagged counterparts. 4. The most dramatic differences between lagged and nonlagged cells appeared in the timing of their responses, as measured by the phase of the response relative to the sinusoidal luminance modulation of a spot centered in the receptive field. Response phase varied approximately linearly with temporal frequency. The slope of the phase versus frequency line is a measure of total integration time, which we refer to as visual latency. Lagged cells has much longer latencies than nonlagged cells. 5. The intercept of the phase versus frequency line is a measure of when in the stimulus cycle the cell responds: we refer to this as the intrinsic or absolute phase of the cell. This measure of response timing not only distinguished lagged and nonlagged cells well but also covaried with the sustained or transient nature of cells' responses to flashed stimuli.(ABSTRACT TRUNCATED AT 400 WORDS)

Temporal-frequency tuning of direction selectivity in cat visual cortex.

Responses of 71 cells in areas 17 and 18 of the cat visual cortex were recorded extracellularly while stimulating with gratings drifting in each direction across the receptive field at a series of temporal frequencies. Direction selectivity was most prominent at temporal frequencies of 1-2 Hz. In about 20% of the total population, the response in the nonpreferred direction increased at temporal frequencies of around 4 Hz and direction selectivity was diminished or lost. In a few cells the preferred direction reversed. One consequence of this behavior was a tendency for the preferred direction to have lower optimal temporal frequencies than the nonpreferred direction. Across the population, the preferred direction was tuned almost an octave lower. In spite of this, temporal resolution was similar in the two directions. It appeared that responses in the nonpreferred direction were suppressed at low frequencies, then recovered at higher frequencies. This phenomenon might reflect the convergence in visual cortex of lagged and nonlagged inputs from the lateral geniculate nucleus. These afferents fire about a quarter-cycle apart (i.e. are in temporal quadrature) at low temporal frequencies, but their phase difference increases to a half-cycle by about 4 Hz. Such timing differences could underlie the prevalence of direction-selective cortical responses at 1 and 2 Hz and the loss of direction selectivity in many cells by 4 or 8 Hz.

Background and stimulus-induced patterns of high metabolic activity in the visual cortex (area 17) of the squirrel and macaque monkey.

We have used 2-deoxy-D-[14C]glucose (2-DG) autoradiography and cytochrome oxidase histochemistry to examine background and stimulus-induced patterns of metabolic activity in monkey striate cortex. In squirrel monkeys (Saimiri sciureus) that binocularly or monocularly viewed diffuse white light or binocularly viewed bars of many orientations and spatial frequencies, 2-DG consumption was not uniform across the cortex but consisted of regularly spaced radial zones of high uptake. The zones extended through all laminae except IVc beta and, when viewed tangentially, formed separate patches 500 microns apart. The cytochrome oxidase stain in these animals also revealed patches of high metabolism which coincided with the 2-DG patches. Squirrel monkeys binocularly viewing vertical stripes showed parallel bands of increased 2-DG uptake in the cortex, while the cytochrome label in these animals remained patchy. When monkeys were kept in the dark during 2-DG exposure, 2-DG-labeled patches were not seen but cytochrome oxidase-positive patches remained. In macaque (Macaca nemestrina) monkeys, binocular stimulation with many orientations and spatial frequencies produced radial zones of high 2-DG uptake in layers I to IVa and VI. When viewed tangentially, these zones formed a dots-in-rows pattern with a spacing of 350 X 500 microns; cytochrome oxidase staining produced an identical pattern. Macaca differed from Saimiri in that monocular stimulation labeled alternate rows. These results indicate that there are radial zones of high background metabolism across squirrel and macaque monkey striate cortex. In Saimiri these zones do not appear to be related to an eye dominance system, while in Macaca they do. The presence of these zones of high metabolism may complicate the interpretation of 2-DG autoradiographs that result from specific visual stimuli.

Strobe rearing reduces direction selectivity in area 17 by altering spatiotemporal receptive-field structure.

Strobe rearing reduces direction selectivity in area 17 by altering spatiotemporal receptive-field structure. J. Neurophysiol. 80: 2991-3004, 1998. Direction selectivity in simple cells of cat area 17 is linked to spatiotemporal (S-T) receptive-field structure. S-T inseparable receptive fields display gradients of response timing across the receptive field that confer a preferred direction of motion. Receptive fields that are not direction selective lack gradients; they are S-T separable, displaying uniform timing across the field. Here we further examine this link using a developmental paradigm that disrupts direction selectivity. Cats were reared from birth to 8 mo of age in 8-Hz stroboscopic illumination. Direction selectivity in simple cells was then measured using gratings drifting at different temporal frequencies (0.25-16 Hz). S-T structure was assessed using stationary bars presented at different receptive-field positions, with bar luminance being modulated sinusoidally at different temporal frequencies. For each cell, plots of response phase versus bar position were fit by lines to characterize S-T inseparability at each temporal frequency. Strobe rearing produced a profound loss of direction selectivity at all temporal frequencies; only 10% of cells were selective compared with 80% in normal cats. The few remaining directional cells were selective over a narrower than normal range of temporal frequencies and exhibited weaker than normal direction selectivity. Importantly, the directional loss was accompanied by a virtual elimination of S-T inseparability. Nearly all cells were S-T separable, like nondirectional cells in normal cats. The loss was clearest in layer 4. Normally, inseparability is greatest there, and it correlates well (r = 0.77) with direction selectivity; strobe rearing reduced inseparability and direction selectivity to very low values. The few remaining directional cells were inseparable. In layer 6 of normal cats, most direction-selective cells are only weakly inseparable, and there is no consistent relationship between the two measures. However, after strobe rearing, even the weak inseparability was eliminated along with direction selectivity. The correlated changes in S-T structure and direction selectivity were confirmed using conventional linear predictions of directional tuning based on responses to counterphasing bars and white noise stimuli. The developmental changes were permanent, being observed up to 12 yr after strobe rearing. The deficits were remarkably specific; strobe rearing did not affect spatial receptive-field structure, orientation selectivity, spatial or temporal frequency tuning, or general responsiveness to visual stimuli. These results provide further support for a critical role of S-T structure in determining direction selectivity in simple cells. Strobe rearing eliminates directional tuning by altering the timing of responses within the receptive field.

Inhibitory contributions to spatiotemporal receptive-field structure and direction selectivity in simple cells of cat area 17.

Intracortical inhibition contributes to direction selectivity in primary visual cortex, but how it acts has been unclear. We investigated this problem in simple cells of cat area 17 by taking advantage of the link between spatiotemporal (S-T) receptive-field structure and direction selectivity. Most cells in layer 4 have S-T-oriented receptive fields in which gradients of response timing across the field confer a preferred direction of motion. Linear summation of responses across the receptive field, followed by a static nonlinear amplification, has been shown previously to account for directional tuning in layer 4. We tested the hypotheses that inhibition acts by altering S-T structure or the static nonlinearity or both. Drifting and counterphasing sine wave gratings were used to measure direction selectivity and S-T structure, respectively, in 17 layer 4 simple cells before and during iontophoresis of bicuculline methiodide (BMI), a GABAA antagonist. S-T orientation was quantified from fits to response temporal phase versus stimulus spatial phase data. Bicuculline reduced direction selectivity and S-T orientation in nearly all cells, and reductions in the two measures were well correlated (r = 0.81) and reversible. Using conventional linear predictions based on response phase and amplitude, we found that BMI-induced changes in S-T structure also accounted well for absolute changes in the amplitude and phase of responses to gratings drifting in the preferred and nonpreferred direction. For each cell we also calculated an exponent used to estimate the static nonlinearity. Bicuculline reduced the exponent in most cells, but the changes were not correlated with reductions in direction selectivity. We conclude that GABAA-mediated inhibition influences directional tuning in layer 4 primarily by sculpting S-T receptive-field structure. The source of the inhibition is likely to be other simple cells with certain spatiotemporal relationships to their target. Despite reductions in the two measures, most receptive fields maintained some directional tuning and S-T orientation during BMI. This suggests that their excitatory inputs, arising from the lateral geniculate nucleus and within area 17, are sufficient to create some S-T orientation and that inhibition accentuates it. Finally, BMI also reduced direction selectivity in 8 of 10 simple cells tested in layer 6, but the reductions were not accompanied by systematic changes in S-T structure. This reflects the fact that S-T orientation, as revealed by our first-order measures of the receptive field, is weak there normally. Inhibition likely affects layer 6 cells via more complex, nonlinear interactions.

Cell types and response timings in the medial interlaminar nucleus and C-layers of the cat lateral geniculate nucleus.

Previous evidence concerning the physiological cell classes in the medial interlaminar nucleus (MIN) has been conflicting. We reexamined the MIN using standard functional tests to distinguish X-, Y- and W-cells. Discharge patterns to flashing spots also were used to identify some cells as lagged or nonlagged, as previously done for the geniculate A-layers. Also, each cell's response timing (latency and absolute phase) was measured from discharges to a spot undergoing sinusoidal luminance modulation. Of 71 MIN cells, 48% were Y, 27% were W, 8% were X, and 17% were unclassifiable. Lagged and nonlagged discharge profiles were observed in each cell group, with 28% of all cells being lagged. Lagged cells displayed a response suppression and long latency to discharge following spot onset, and a slow decay in firing at spot offset that was often preceded by a transient discharge. These profiles were indistinguishable from those of lagged cells in the A-layers. MIN cells also were heterogeneous in response timing, displaying a range of latency and absolute phase values similar to that in the A-layers. We extended these analyses to 27 cells in the geniculate C-layers. In layer C, 35% of cells were Y, 10% were X, 25% were W, and 30% were unclassifiable. About 11% had lagged profiles, and were X-cells or unclassifiable cells. Layers C1 and C2 contained only W-cells and no lagged profiles. The range of timings in the C-layers was somewhat narrower than in the MIN. Overall, these results show that the MIN contains a greater variety of functional cell classes than heretofore appreciated. Further, it appears that mechanisms which create different timing delays in the A-layers also exist in the MIN and layer C. These timings may contribute to direction selectivity in extrastriate cortex.

Lagged Y cells in the cat lateral geniculate nucleus.

We report on the existence of lagged Y (YL) cells in the A laminae of the cat lateral geniculate nucleus (LGN) and on criteria for identifying them using visual and electrical stimulation. Like the lagged X (XL) cells described previously (Mastronarde, 1987a; Humphrey & Weller, 1988a), YL cells responded to a spot stimulus with an initial dip in firing and a delayed latency to discharge after spot onset, and an anomalously prolonged firing after spot offset. However, the cells received excitatory input from retinal Y rather than X afferents, and showed nonlinear spatial summation and other Y-like receptive-field properties. Three YL cells tested for antidromic activation from visual cortex were found to be relay cells, with long conduction latencies similar to those of XL cells. Simultaneous recordings of a YL cell and its retinal Y afferents show striking parallels between lagged X and Y cells in retinogeniculate functional connectivity, and suggest that the YL-cell response profile reflects inhibitory processes occurring within the LGN. The YL cells comprised approximately 5% of Y cells and approximately 1% of all cells in the A laminae. Although infrequently encountered in the LGN, they may be roughly as numerous as Y cells in the retina, and hence could fulfill an important role in vision.

Monocular deprivation affects X- and Y-cell retinogeniculate terminations in cats.

The X- and Y-cell pathways in cats form two functionally distinct, parallel systems from the retina through the lateral geniculate nucleus (LGN) to the visual cortex1-4. We recently used the technique of intraaxonal injection of horseradish peroxidase (HRP) to demonstrate major differences between X- and Y-cells in their retinogeniculate termination patterns5 (compare Figs 1 alpha and 2 alpha). Normally, axons of X-cells innervate geniculate lamina A or A1 (depending on the eye of origin) in narrow zones oriented perpendicular to the lamination. Some X-cells also terminate sparsely (that is, with few boutons) in the medial interlaminar nucleus (MIN), a subdivision of the LGN. Y-cell axons terminate either in laminae C and A (from the contralateral retina) or in lamina A1 (from the ipsilateral retina) in broad zones5,6, and most also terminate densely (with many boutons) in the MIN. We now report that cats raised with monocular lid suture develop abnormal retinogeniculate termination patterns. Many X-cell axons arising from the deprived eye have unusually broad terminal fields in lamina A or A1, and some also densely innervate the MIN. Many Y-cell axons from the deprived eye have dramatically shrunken or absent terminal fields in the A laminae and MIN. These changes constitute the most peripheral effects of monocular deprivation discovered so far, are consistent with previous reports of functional abnormalities among deprived geniculate neurones4,7,8 ad suggest possible mechanisms by which the visual environment influences neuronal development.