Thalamocortical specificity and the synthesis of sensory cortical receptive fields

A persistent and fundamental question in sensory cortical physiology concerns the manner in which receptive fields of layer-4 neurons are synthesized from their thalamic inputs. According to a hierarchical model proposed more than 40 years ago, simple receptive fields in layer 4 of primary visual cortex originate from the convergence of highly specific thalamocortical inputs (e.g., geniculate inputs with on-center receptive fields overlap the on subregions of layer 4 simple cells). Here, we summarize studies in the visual cortex that provide support for this high specificity of thalamic input to visual cortical simple cells. In addition, we review studies of GABAergic interneurons in the somatosensory "barrel" cortex with receptive fields that are generated by a very different mechanism: the nonspecific convergence of thalamic inputs with different response properties. We hypothesize that these 2 modes of thalamocortical connectivity onto subpopulations of excitatory and inhibitory neurons constitute a general feature of sensory neocortex and account for much of the diversity seen in layer-4 receptive fields.     

Receptive field size and response latency are correlated within the cat visual thalamus

Each point in visual space is encoded at the level of the thalamus by a group of neighboring cells with overlapping receptive fields. Here we show that the receptive fields of these cells differ in size and response latency but not at random. We have found that in the cat lateral geniculate nucleus (LGN) the receptive field size and response latency of neighboring neurons are significantly correlated: the larger the receptive field, the faster the response to visual stimuli. This correlation is widespread in LGN. It is found in groups of cells belonging to the same type (e.g., Y cells), and of different types (i.e., X and Y), within a specific layer or across different layers. These results indicate that the inputs from the multiple geniculate afferents that converge onto a cortical cell (approximately 30) are likely to arrive in a sequence determined by the receptive field size of the geniculate afferents. Recent studies have shown that the peak of the spatial frequency tuning of a cortical cell shifts toward higher frequencies as the response progresses in time. Our results are consistent with the idea that these shifts in spatial frequency tuning arise from differences in the response time course of the thalamic inputs.     

Area 18 corticotectal cells: response properties and identification of sustaining geniculate inputs

1. We examined the response properties and geniculate inputs of 35 antidromically identified corticotectal (CT) cells within area 18 of the paralyzed, anesthetized cat. Twenty-three were either standard complex or hypercomplex, 11 were special complex, and 1 was simple. 2. The response properties of CT cells in area 18 were in general quite similar to those examined in a previous study of area 17 CT cells, including similar proportions of standard and special complex CT cells, virtually identical length-response functions, and similar orientation and direction tuning. 3. Area 18 CT cells are rapidly conducting. They are considerably faster than area 17 CT cells. 4. We investigated the composition of thalamic inputs to CT cells by reversibly inactivating a portion of layer A and/or the C layers of the dorsal lateral geniculate nucleus with injections of cobaltous chloride. Blocking layer A strongly attenuated the visual responsiveness of about half of the cells tested. Blocking the C layers alone generally had only moderate effects, but simultaneous blockade of layer A and the C layers demonstrated a substantial C-layer input to many cells. Unlike area 17 in which there is a strong correlation between CT cell class and dependence on layer A, no single receptive-field parameter nor set of parameters was correlated with dependence on layer A. However, cells least affected by simultaneous blockade of layer A and the C layers were special complex, suggesting that, as in area 17, area 18 special complex CT cells integrate more geniculate inputs than standard complex CT cells. 5. We propose that the similarities of response properties of area 17 and area 18 CT cells results from their participation in similar interlaminar columnar circuits and that differences in the patterns of geniculate control reflect differences in the global patterns of geniculate inputs to these two areas.     

Functional independence of layer IV barrels in rodent somatosensory cortex.

Layer IV of rodent primary somatosensory cortex is characterized by an array of whisker-related groups of neurons, known as "barrels." Neurons within each barrel respond best to a particular whisker on the contralateral face, and, on deflection of adjacent whiskers, display relatively weak excitation followed by strong inhibition. A prominent hypothesis for the processing of vibrissal information within layer IV is that the multiwhisker receptive fields of barrel neurons reflect interconnections among neighboring barrels. An alternative view is that the receptive field properties of barrel neurons are derived from operations performed on multiwhisker, thalamic inputs by local circuitry within each barrel, independently of neighboring barrels. Here we report that adjacent whisker-evoked excitation and inhibition within a barrel are unaffected by ablation of the corresponding adjacent barrel. In supragranular neurons, on the other hand, excitatory responses to the ablated barrel's associated whisker are substantially reduced. We conclude that the layer IV barrels function as an array of independent parallel processors, each of which individually transforms thalamic afferent input for subsequent processing by horizontally interconnected circuits in other layers.     

Population receptive fields of ON and OFF thalamic inputs to an orientation column in visual cortex

The primary visual cortex of primates and carnivores is organized into columns of neurons with similar preferences for stimulus orientation, but the developmental origin and function of this organization are still matters of debate. We found that the orientation preference of a cortical column is closely related to the population receptive field of its ON and OFF thalamic inputs. The receptive field scatter from the thalamic inputs was more limited than previously thought and matched the average receptive field size of neurons at the input layers of cortex. Moreover, the thalamic population receptive field (calculated as ON - OFF average) had separate ON and OFF subregions, similar to cortical neurons in layer 4, and provided an accurate prediction of the preferred orientation of the column. These results support developmental models of orientation maps that are based on the receptive field arrangement of ON and OFF visual inputs to cortex.     

Receptive fields and response properties of neurons in layer 4 of ferret visual cortex

The ferret has become a model animal for studies exploring the development of the visual system. However, little is known about the receptive-field structure and response properties of neurons in the adult visual cortex of the ferret. We performed single-unit recordings from neurons in layer 4 of adult ferret primary visual cortex to determine the receptive-field structure and visual-response properties of individual neurons. In particular, we asked what is the spatiotemporal structure of receptive fields of layer 4 neurons and what is the orientation selectivity of layer 4 neurons? Receptive fields of layer 4 neurons were mapped using a white-noise stimulus; orientation selectivity was determined using drifting, sine-wave gratings. Our results show that most neurons (84%) within layer 4 are simple cells with elongated, spatially segregated, ON and OFF subregions. These neurons are also selective for stimulus orientation; peaks in orientation-tuning curves have, on average, a half-width at half-maximum response of 21.5 +/- 1.2 degrees (mean +/- SD). The remaining neurons in layer 4 (16%) lack orientation selectivity and have center/surround receptive fields. Although the organization of geniculate inputs to layer 4 differs substantially between ferret and cat, our results demonstrate that, like in the cat, most neurons in ferret layer 4 are orientation-selective simple cells.     

Synaptic properties of thalamic input to layers 2/3 and 4 of primary somatosensory and auditory cortices

We studied the synaptic profile of thalamic inputs to cells in layers 2/3 and 4 of primary somatosensory (S1) and auditory (A1) cortices using thalamocortical slices from mice age postnatal days 10-18. Stimulation of the ventral posterior medial nucleus (VPM) or ventral division of the medial geniculate body (MGBv) resulted in two distinct classes of responses. The response of all layer 4 cells and a minority of layers 2/3 cells to thalamic stimulation was Class 1, including paired-pulse depression, all-or-none responses, and the absence of a metabotropic component. On the other hand, the majority of neurons in layers 2/3 showed a markedly different, Class 2 response to thalamic stimulation: paired-pulse facilitation, graded responses, and a metabotropic component. The Class 1 and Class 2 response characteristics have been previously seen in inputs to thalamus and have been described as drivers and modulators, respectively. Driver input constitutes a main information bearing pathway and determines the receptive field properties of the postsynaptic neuron, whereas modulator input influences the response properties of the postsynaptic neuron but is not a primary information bearing input. Because these thalamocortical projections have comparable properties to the drivers and modulators in thalamus, we suggest that a driver/modulator distinction may also apply to thalamocortical projections. In addition, our data suggest that thalamus is likely to be more than just a simple relay of information and may be directly modulating cortex.     

Thalamo-cortical connections and their correlation with receptive field properties in the cat's lateral suprasylvian visual cortex

Summary Areas PMLS and PLLS of the cat's lateral suprasylvian visual cortex display an interesting global organization of local features in their single unit response properties: direction preference is centrifugally organized and velocity preference increases with eccentricity. In addition it has previously been shown that binocular interactions are strongest around the visual field center. This characterizes the LS areas as apt for the analysis of optic flow fields and for visual processing in various kinds of visuomotor tasks (Rauschecker et al. 1987). In the present study we analysed the types of input to LS from the optic chiasm, the corpus callosum and from two thalamic relay nuclei (lateral posterior and lateral geniculate) that constitute important sources of afferent information to the LS areas. We were interested in learning how the afferent (and efferent) connections between LS and these structures relate to the response properties of LS neurons. Overlap of an RF into the ipsilateral hemifield was virtually always associated with callosal input. Latency differences between responses to electrical stimulation of the optic chiasm and the thalamic sites indicated almost exclusively fast-conducting Y-input to LS. Correlation of response latencies with receptive field properties revealed the following correspondences: A positive correlation was found between LP-latency and RF-size matching the dependence of RF size on laminar origin. The type of correlation found between LP-latency and directional tuning of LS cells suggests that an interaction between thalamic and other inputs may be responsible for direction selectivity in LS. Finally, correlation of LP-latencies with centrifugal direction preference suggests that this specific property is generated by intracortical wiring rather than by thalamic input.     

Receptive-field properties and laminar distribution of X-like and Y-like simple cells in cat area 17

We examined the spatiotemporal organization of excitatory regions in 197 simple receptive fields from cat area 17 using the peristimulus time response-plane technique of Stevens and Gerstein (53). With this method we observed a striking similarity between the spatiotemporal organization of excitatory regions in simple receptive fields and the excitatory centers in X or Y geniculate receptive fields. This observation suggested to us the possibility that individual simple receptive fields may be differentially innervated by either X or Y geniculate afferents. To test this hypothesis, we devised a quantitative measure that could characterize the excitatory regions in simple receptive fields as being X-like or Y-like. This measure was based on an understanding of the spatiotemporal organization of geniculate X and Y receptive fields. Further evidence supporting this division of simple cells was derived from additional physiological and anatomical comparisons. When compared to Y-like simple cells, X-like simple cells, as a group, gave a more sustained response to standing contrast, had smaller excitatory regions, and preferred slightly slower moving stimuli. A comparison of the properties of end-zone inhibition and directional selectivity showed no additional difference between X-like and Y-like simple cells. We found a correlation between the laminar position of X-like and Y-like simple cells and the known patterns of termination of X and Y geniculate afferents. Y-like simple cells were found in layers III, IVab, and VI, but not in layer IVc, whereas X-like simple cells were found in layer III, all parts of layer IV, and layer VI. Inhibitory regions appeared to play a major role in defining the spatiotemporal structure of simple receptive fields and they further acted to diminish differences between the spatial widths and velocity sensitivities of X-like and Y-like simple cells. These data are discussed in terms of a parallel model of geniculostriate convergence and support the hypothesis that the X and Y systems, which originate in the retina, are maintained in parallel at the level of simple cells in striate cortex.     

Diverse receptive fields in the lateral geniculate nucleus during thalamocortical development

Most models of thalamocortical development in the visual system assume a homogeneous population of thalamic inputs to the cortex, each with concentric on- or off-center receptive fields. To test this, we made high-resolution spatial maps of receptive fields in the developing ferret lateral geniculate nucleus (LGN). Developing receptive fields (RFs), had a variety of shapes: some concentric, others elongated (like adult cortical receptive fields) and some with 'hot spots' of sensitivity. These receptive fields seemed to arise from convergence of multiple retinal afferents onto LGN neurons. We present a Hebbian model whereby imprecise retinogeniculate connections help refine geniculocortical connections, sharpening both thalamocortical topography and perhaps orientation selectivity.     

Properties of a population of GABAergic cells in murine auditory cortex weakly excited by thalamic stimulation

Feedforward inhibition triggered by thalamocortical (TC) afferents sharpens onset responses and shapes receptive fields of pyramidal cells in auditory cortex (ACx). Previous studies focused only on interneurons located in and around layer IV in primary ACx, target of the dense thalamic projections from ventral medial geniculate. We investigated a population of feedforward interneurons located throughout layers I-V and activated by both afferents from primary and nonprimary thalamus using recordings from auditory TC brain slices obtained from mice expressing green fluorescent protein under control of the glutamic acid decarboxylase (GAD65) promoter in a subpopulation of cortical GABAergic cells. We studied the responses of these interneurons and of pyramidal cells in ACx to thalamic stimulation and to hyper- and depolarizing current pulses. Most interneurons exhibited monosynaptic responses to thalamic stimulation, but this excitation was weak and subthreshold. Interneurons had multipolar dendritic morphology with widespread and dense axonal projections extending several hundred micrometers from the soma. In pyramidal cells from layers II-IV, thalamic excitatory postsynaptic potentials were significantly larger than in interneurons and were superthreshold in 40% of cells, but in these cells, there was no evidence of feedforward inhibition. By contrast, feedforward inhibition was observed in 12 of 18 layer V pyramidal cells. Thus feedforward inhibition in supragranular layers of ACx is weak, and these interneurons require coincident excitation to be activated by thalamic inputs.     

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.     

Cortical columnar processing in the rat whisker-to-barrel system.

Controlled whisker stimulation and single-unit recordings were used to elucidate response transformations that occur during the processing of tactile information from ventral posterior medial thalamus (VPM) through cortical columns in the rat whisker/barrel cortex. Whiskers were either deflected alone, using punctate ramp-and-hold stimuli, or in combination with a random noise vibration applied simultaneously to two or more neighboring whiskers. Quantitative data were obtained from five anatomically defined groups of neurons based on their being located in: VPM, layer IV barrels, layer IV septa, supragranular laminae, and infragranular laminae. Neurons in each of these populations displayed characteristic properties related to their response latency and time course, relative magnitudes of responses evoked by stimulus onset versus offset, strength of excitatory responses evoked by the noise stimulus, and/or the degree to which the noise stimulus, when applied to neighboring whiskers, suppressed or facilitated responses evoked by the columnar whisker. Results indicate that within layer IV itself there are at least two anatomically distinct networks, barrel and septum, that independently process afferent information, transforming thalamic input in similar but quantitatively distinguishable ways. Transformed signals are passed on to circuits in supragranular and infragranular laminae. In the case of supragranular neurons, evidence suggests that circuits there function in a qualitatively different fashion from those in layer IV, diminishing response differentials between weak and strong inputs, rather than enhancing them. Compared to layer IV, the greater heterogeneity of receptive field properties in nongranular layers suggests the existence of multiple, operationally distinct local circuits in the output layers of the cortical column.     

Laminar differences in receptive field properties of cells in cat primary visual cortex

1. Cells in area 17 of the cat visual cortex were studied with a view towards correlating receptive field properties with layering. A number of receptive field parameters were measured for all units, and nearly every unit was marked with a microlesion to determine accurately the layer in which it was found.

2. Cells were defined as simple or complex by mapping with stationary stimuli, using the criteria of Hubel & Wiesel (1962). Complex cells fell into two groups: those that showed summation for increased slit length (standard complex) and those that did not (special complex).

3. The simple cells were located in the deep part of layer 3, in layer 4, and in layer 6. This corresponds to the distribution of afferents from the dorsal layers of the lateral geniculate nucleus. In these cortical layers the simple cells differed primarily with respect to their receptive field size, cells in layer 4 having the smallest, layer 3 intermediate, and layer 6 the largest fields. Layer 4 was the only layer in which simple cells showed end-inhibition (a reduction in response to slits extending beyond the excitatory portion of the receptive field).

4. The standard complex cells were found in all layers, but were quite scarce in layer 4. As with the simple cells, field size varied with layer: in layer 2+3 they had small to intermediate field sizes, in layer 5 intermediate, and in layer 6 very large. Layer 6 cells showed summation for slits of increased length up to very large values, and responded best when the slits were centred in the receptive field.

The only standard complex cells that showed end-inhibition were those in layer 2+3, and these were similar to the layer 4 simple cells in terms of proportion of end-inhibited units and degree of end-inhibition.

5. The special complex cells, originally described by Palmer & Rosenquist (1974), were found in two tiers: the upper one at the layer 3/layer 4 border and the lower one in layer 5. They were different from the standard complex cells in having a high spontaneous activity, high velocity preference, and large fields which were similar in size (at a given eccentricity) from one cell to the next. Many showed reduced response to slits of increasing length, even for slits that did not extend beyond the borders of the responsive region.

6. Cells in layer 6 (the origin of the corticogeniculate projection) were antidromically activated from the lateral geniculate nucleus. The antidromically activated units included both simple and complex cells, and they had the long receptive fields characteristic of the overall population of cells in layer 6.

7. The results showed that there are different types of simple and complex cells, and that cells in different layers have different properties. Taken together with their differences in site of projection, this demonstrates that the anatomical lamination pattern is reflected in functional differences between cells in different layers.

     

Dynamics of the orientation-tuned membrane potential response in cat primary visual cortex

Neurons in the primary visual cortex are highly selective for stimulus orientation, whereas their thalamic inputs are not. Much controversy has been focused on the mechanism by which cortical orientation selectivity arises. Although an increasing amount of evidence supports a linear model in which orientation selectivity is conferred upon visual cortical cells by the alignment of the receptive fields of their thalamic inputs, the controversy has recently been rekindled with the suggestion that late cortical input--delayed by multiple synapses--could lead to sharpening of orientation selectivity over time. Here we used intracellular recordings in vivo to examine temporal properties of the orientation-selective response to flashed gratings. Bayesian parameter estimation demonstrated that both preferred orientation and tuning width were stable throughout the response to a single stimulus.     

Contrasts in spatial organization of receptive fields at geniculate and retinal levels: centre surround and outer surround

1. The organization of receptive fields of retinal ganglion cells and A-laminae cells from the dorsal lateral geniculate nucleus (LGN) of the cat are compared under identical conditions. Some aspects of the geniculate data have been given elsewhere (Hammond, 1972b).2. The receptive fields of geniculate cells consist of three zones - centre, antagonistic surround and synergistic outer surround - compared with only two for retinal cells. This result further supports the theory that the centre and surround of geniculate cell receptive fields derive from convergent, but discrete, retinal inputs.3. The surrounds of geniculate receptive fields are known to be more powerfully antagonistic on their centres than is true of retinal cells. This relationship is re-examined.4. Unlike geniculate fields, the locus of maximum sensitivity for the receptive field surround of retinal cells is not invariant either to stimulus geometry or adaptational state.5. The latter result strongly suggests that the surround mechanism for retinal cells extends through the centre of the field. It establishes unequivocally that the overlap between receptive field centre and surround mechanisms, only marginal in geniculate, is very extensive indeed in retina.     

The differential distribution of the growth-associated protein-43 in first and higher order thalamic nuclei of the adult rat

Corticothalamic axons from layer 5 of primary and secondary auditory and visual areas have large terminals that make multiple synaptic contacts on proximal dendrites of relay cells in higher order thalamic nuclei and have been termed "driver" inputs. The corticothalamic cells express mRNA for the presynaptic growth-associated protein-43, in the adult rat [Feig SL (2004) Corticothalamic cells in layers 5 and 6 of primary and secondary sensory cortex express GAP-43 mRNA in the adult rat. J Comp Neurol 468:96-111]. In contrast, ascending driver afferents to first order nuclei (e.g. retinal, inferior collicular, and lemniscal) lose growth-associated protein-43 as mature synaptic terminals are established. Levels of immunoreactivity for growth-associated protein-43 are compared for first and higher order visual (lateral geniculate and lateral posterior), auditory (ventral and dorsal divisions of the medial geniculate), and somatosensory (ventral posterior and posterior) thalamic nuclei. At one week postnatal, staining for growth-associated protein-43 is uniform throughout first and higher order thalamic nuclei. By three weeks and thereafter, staining is denser in the higher order than first order thalamic nuclei. Electron microscopy shows growth-associated protein-43 in profiles with characteristics of afferents from layer 5 in LP and medial geniculate nucleus and no such label in retinal afferents in lateral geniculate nucleus. In these nuclei, approximately 25% of the profiles with characteristics of cortical afferents from layer 6 have label for growth-associated protein-43. The superficial layers of the superior colliculus also show growth-associated protein-43 positive profiles with characteristics of terminals from cortical layer 5. Some growth-associated protein-43 positive terminals were also positive for GABA in the thalamic nuclei studied and in the superior colliculus. The data suggest that sensory afferents to first order thalamocortical relays become stabilized once mature synaptic patterns are established, but the higher stages of information processing involving higher order thalamic relays, via cells in cortical layer 5, retain plasticity related to growth-associated protein-43 in the adult.     

The inhibitory role of the visually responsive region of the thalamic reticular nucleus in the rat

Summary Two-shock inhibition, a feature of 98 of 100 P cells recorded in the dorsal lateral geniculate nucleus of the normal rat, was not observed in 91 of 140 geniculate cells after an electrolytic lesion had been made in the adjacent visually responsive thalamic reticular nucleus. Nine geniculate cells recorded both before and after a reticular lesion had their initial inhibition abolished or substantially reduced after the lesion. The reticular lesion eliminated the bursts of spikes which normally terminate periods of inhibition following electrical or photic stimulation but caused no other changes in receptive field organization of geniculate cells. We conclude that the visually responsive region of the thalamic reticular nucleus in the rat is responsible for the profound two-shock inhibition and for the post-inhibitory bursts which are normal properties of relay cells of the dorsal lateral geniculate nucleus.     

Corticotectal circuit in the cat: a functional analysis of the lateral geniculate nucleus layers of origin

1. The dorsal lateral geniculate nucleus (LGN) of the cat is a major thalamic relay between the retina and several visual cortical areas. These cortical areas in turn project to the superior colliculus (SC). The aim of the present experiment was to determine which LGN layers provide a necessary input to the corticotectal circuit. 2. Individual layers of the LGN were reversibly inactivated by microinjection of cobalt chloride during recording of visual responses in the retinotopically corresponding part of the superior colliculus. 3. For cells driven through the contralateral eye, inactivation of layer A or the medial interlaminar nucleus (MIN) had little effect on visual responsiveness in the superior colliculus. In contrast, inactivation of layer C abolished visual responses at one-quarter of the SC recording sites, reduced responses at another quarter, and left half of the recording sites unaffected. 4. For cells driven through the ipsilateral eye, inactivation of layer C1 or the MIN had no effect. Inactivation of layer A1 uniformly reduced visual responses in the superior colliculus and usually abolished them entirely. 5. These results are compatible with previous work showing that cortical input to the SC originates from Y-cells. They indicate that two of the five Y-cell containing layers (A1 and C) provide major inputs to the corticotectal circuit. The results suggest that layer A1 is functionally allied to layer C as well as to layer A.     

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)