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R Clay Reid

Publications and source records attributed to R Clay Reid.

10 recordsLinked to original sources

Single-neuron responses and neuronal decisions in a vernier task.

Vernier acuity is a measure of the smallest horizontal offset between two vertical lines that can be behaviorally discriminated. To examine the link between the neuronal responses in a retinotopic mosaic and vernier acuity, we recorded the responses of single cells in cat lateral geniculate nucleus to a vertical bar stimulus that was stepped in small increments through the receptive fields of cells. Based on the single-trial responses evoked by stimuli at different positions, we calculated the spatial resolution that could be achieved. If the stimulus could fall anywhere in their receptive fields, single neurons had spatial resolutions two times worse than previously reported vernier thresholds. Given the known coverage factor in a cat retina, we developed a two-stage decision model to examine how the responses of neurons in a retinotopic mosaic could be processed to achieve vernier acuity. In order for psychophysical thresholds to be accounted for by the responses of a single cell, the stimulus must fall in the quarter of the receptive field that provides the most information about stimulus position. Alternatively, both the absolute psychophysical threshold for vernier acuity and its dependence on stimulus length can be realized by pooling the responses of a few neurons, all located on one side of the bar stimulus.

Action Potentials↗

Receptive field structure varies with layer in the primary visual cortex.

Here we ask whether visual response pattern varies with position in the cortical microcircuit by comparing the structure of receptive fields recorded from the different layers of the cat's primary visual cortex. We used whole-cell recording in vivo to show the spatial distribution of visually evoked excitatory and inhibitory inputs and to stain individual neurons. We quantified the distribution of 'On' and 'Off' responses and the presence of spatially opponent excitation and inhibition within the receptive field. The thalamorecipient layers (4 and upper 6) were dominated by simple cells, as defined by two criteria: they had separated On and Off subregions, and they had push-pull responses (in a given subregion, stimuli of the opposite contrast evoked responses of the opposite sign). Other types of response profile correlated with laminar location as well. Thus, connections unique to each visual cortical layer are likely to serve distinct functions.

Action Potentials↗

Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex.

Neurons in the cerebral cortex are organized into anatomical columns, with ensembles of cells arranged from the surface to the white matter. Within a column, neurons often share functional properties, such as selectivity for stimulus orientation; columns with distinct properties, such as different preferred orientations, tile the cortical surface in orderly patterns. This functional architecture was discovered with the relatively sparse sampling of microelectrode recordings. Optical imaging of membrane voltage or metabolic activity elucidated the overall geometry of functional maps, but is averaged over many cells (resolution >100 microm). Consequently, the purity of functional domains and the precision of the borders between them could not be resolved. Here, we labelled thousands of neurons of the visual cortex with a calcium-sensitive indicator in vivo. We then imaged the activity of neuronal populations at single-cell resolution with two-photon microscopy up to a depth of 400 microm. In rat primary visual cortex, neurons had robust orientation selectivity but there was no discernible local structure; neighbouring neurons often responded to different orientations. In area 18 of cat visual cortex, functional maps were organized at a fine scale. Neurons with opposite preferences for stimulus direction were segregated with extraordinary spatial precision in three dimensions, with columnar borders one to two cells wide. These results indicate that cortical maps can be built with single-cell precision.

Analysis of Variance↗

Efficacy of retinal spikes in driving cortical responses.

How does a single retinal ganglion cell (RGC) affect the firing of simple cells in the visual cortex? Although much is known of the functional connections between the retina and the lateral geniculate nucleus (LGN) and between LGN and visual cortex, it is hard to infer the effect of disynaptic connections from retina to visual cortex. Most importantly, there is considerable divergence from retina to LGN, so cortical neurons might be influenced by ganglion cells through multiple feedforward pathways. We recorded simultaneously from ganglion cells in the retina and cortical simple cells in the striate cortex with overlapping receptive fields and evaluated disynaptic connections with cross-correlation analysis. In all disynaptically connected pairs, the retinal receptive field center and overlapping cortical subregion always shared the same sign (either both ON or both OFF). Connected pairs were similar in other respects, such as relative position and timing of their receptive fields, and thus obeyed the same rules of connectivity found previously for retinothalamic and thalamocortical connections. We found that a single RGC directly contributed on average to approximately 3% of the activity of its cortical target. The relative timing of pairs of spikes from the retinal cell affected their efficacy in driving the cortical cell. When two retinal spikes were closely spaced (<10 msec), the second spike was several times more likely to drive the cortical target. The relative magnitude of this disynaptic paired spike enhancement was considerably larger than has been found previously for retinogeniculate and geniculocortical connections. The amplified paired spike enhancement from retina to cortex ensures that signal transmission from retina to cortex is particularly effective when the retina fires a series of closely spaced action potentials.

Action Potentials↗

Role of subplate neurons in functional maturation of visual cortical columns.

The subplate forms a transient circuit required for development of connections between the thalamus and the cerebral cortex. When subplate neurons are ablated, ocular dominance columns do not form in the visual cortex despite the robust presence of thalamic axons in layer 4. We show that subplate ablation also prevents formation of orientation columns. Visual responses are weak and poorly tuned to orientation. Furthermore, thalamocortical synaptic transmission fails to strengthen, whereas intracortical synapses are unaffected. Thus, subplate circuits are essential not only for the anatomical segregation of thalamic inputs but also for key steps in synaptic remodeling and maturation needed to establish the functional architecture of visual cortex.

Animals↗

The spatial receptive field of thalamic inputs to single cortical simple cells revealed by the interaction of visual and electrical stimulation.

Electrical stimulation of the thalamus has been widely used to test for the existence of monosynaptic input to cortical neurons, typically with stimulation currents that evoke cortical spikes with high probability. We stimulated the lateral geniculate nucleus (LGN) of the thalamus and recorded monosynaptically evoked spikes from layer 4 neurons in visual cortex. We found that with moderate currents, cortical spikes were evoked with low to moderate probability and their occurrence was modulated by ongoing sensory (visual) input. Furthermore, when repeated at 8-12 Hz, electrical stimulation of the thalamic afferents caused such profound inhibition that cortical spiking activity was suppressed, aside from electrically evoked monosynaptic spikes. Visual input to layer 4 cortical cells between electrical stimuli must therefore have derived exclusively from LGN afferents. We used white-noise visual stimuli to make a 2D map of the receptive field of each cortical simple cell during repetitive electrical stimulation in the LGN. The receptive field of electrically evoked monosynaptic spikes (and thus of the thalamic input alone) was significantly elongated. Its primary subfield was comparable to that of the control receptive field, but secondary (flanking) subfields were weaker. These findings extend previous results from intracellular recordings, but also demonstrate the effectiveness of an extracellular method of measuring subthreshold afferent input to cortex.

Afferent Pathways↗

Saccadic eye movements modulate visual responses in the lateral geniculate nucleus.

We studied the effects of saccadic eye movements on visual signaling in the primate lateral geniculate nucleus (LGN), the earliest stage of central visual processing. Visual responses were probed with spatially uniform flickering stimuli, so that retinal processing was uninfluenced by eye movements. Nonetheless, saccades had diverse effects, altering not only response strength but also the temporal and chromatic properties of the receptive field. Of these changes, the most prominent was a biphasic modulation of response strength, weak suppression followed by strong enhancement. Saccadic modulation was widespread, and affected both of the major processing streams in the LGN. Our results demonstrate that during natural viewing, thalamic response properties can vary dramatically, even over the course of a single fixation.

Action Potentials↗

Precise firing events are conserved across neurons.

Sensory neurons can respond to dynamic stimuli with temporally precise firing events. In the lateral geniculate nucleus (LGN) of the thalamus, we found previously that when a flickering visual stimulus was repeated, individual cells fired action potentials at the same time in every trial to within 1 msec. We now show that these precise firing events are also reproducible across cells of the same class. Therefore, the mechanisms for producing precise timing must be conserved within a cell class. Our results further suggest that cortical neurons would require only a few generic processing mechanisms to extract the fine temporal information available in their LGN inputs.

Action Potentials↗

Space and time maps of cone photoreceptor signals in macaque lateral geniculate nucleus.

We studied neurons in the central visual field representation of the lateral geniculate nucleus (LGN) in macaque monkeys by mapping their receptive fields in space and time. The mapping was performed by reverse correlation of a spike train of a neuron with pseudorandom, binary level stimuli (m-sequence grids). Black and white m-sequence grids were used to map the receptive field for luminance. The locations of receptive field center and surround were determined from this luminance map. To map the contribution of each cone class to the receptive field, we designed red-green or blue-yellow m-sequence grids to isolate the influence of that cone (long, middle, or short wavelength-sensitive: L, M, or S). Magnocellular neurons generally received synergistic input from L and M cones in both the center and the surround. A minority had cone-antagonistic (M-L) input to the surround. Red-green opponent parvocellular neurons received opponent cone input (L+M- or M+L-) that overlapped in space, as sampled by our stimulus grid, but that had somewhat different extents. For example, an L+ center parvocellular neuron would be L+/M- in both center and surround, but the L+ signal would be stronger in the center and the M- signal stronger in the surround. Accordingly, the luminance receptive field would be spatially antagonistic: on-center/off-surround. The space-time maps also characterized LGN dynamics. For example, magnocellular responses were transient, red-green parvocellular responses were more sustained, and blue-on responses were the most sustained for both luminance and cone-isolating stimuli. For all cell types the surround response peaked 8-10 msec later than the center response.

Action Potentials↗

Laminar processing of stimulus orientation in cat visual cortex.

One of the most salient features to emerge in visual cortex is sensitivity to stimulus orientation. Here we asked if orientation selectivity, once established, is altered by successive stages of cortical processing. We measured patterns of orientation selectivity at all depths of the cat's visual cortex by making whole-cell recordings with dye-filled electrodes. Our results show that the synaptic representation of orientation indeed changes with position in the microcircuit, as information passes from layer 4 to layer 2+3 to layer 5. At the earliest cortical stage, for simple cells in layer 4, orientation tuning curves for excitation (depolarization) and inhibition (hyperpolarization) had similar peaks (within 0-7 deg, n = 11) and bandwidths. Further, the sharpness of orientation selectivity covaried with receptive field geometry (r = 0.74) - the more elongated the strongest subregion, the shaper the tuning. Tuning curves for complex cells in layer 2+3 also had similar peaks (within 0-4 deg, n = 7) and bandwidths. By contrast, at a later station, layer 5, the preferred orientation for excitation and inhibition diverged such that the peaks of the tuning curves could be as far as 90 deg apart (average separation, 54 deg; n = 6). Our results support the growing consensus that orientation selectivity is generated at the earliest cortical level and structured similarly for excitation and inhibition. Moreover, our novel finding that the relative tuning of excitation and inhibition changes with laminar position helps resolve prior controversy about orientation selectivity at later phases of processing and gives a mechanistic view of how the cortical circuitry recodes orientation.

Action Potentials↗