Judith A. Hirsch

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 cats 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.

Long-term changes in synaptic strength along specific intrinsic pathways in the cat visual cortex.

1. The dense system of horizontal connections that arise and course within the striate cortex are thought to inform single cells about stimuli arising in disparate points in visual space and to modulate responses evoked from within the receptive field. To learn whether or not the strength of the horizontal connections could vary over the long term, and if such changes could affect the integration of vertical, interlaminar inputs, we have recorded intracellularly from the superficial layers in slices of the adult cats visual cortex. 2. The monosynaptic EPSP evoked by stimulating horizontal fibres showed long‐term facilitation in twelve of the twenty cells that were conditioned by repetitively pairing synaptic responses with depolarizing pulses of current; the maximum increase observed was 200%. Strong inhibition present in the postsynaptic response usually indicated that facilitation would not occur. 3. In instances where horizontal input evoked both mono‐ and polysynaptic EPSPs, both early and late events showed facilitation, with the most dramatic enhancement contributed by the polysynaptic components. 4. For the twenty‐eight cells whose responses to stimulation of interlaminar as well as horizontal pathways were assessed, all were found to receive non‐overlapping inputs from each source. Conditioning produced long‐term changes in the strength of the interlaminar inputs. 5. Changes in synaptic strength were usually confined to the conditioned pathway, though in four out of twenty‐six times we observed heterosynaptic facilitation of polysynaptic EPSPs. 6. The conditioning protocol led to lasting depression rather than facilitation in three out of eleven instances; the reduction was only observed in the multisynaptic components. 7. We suggest that the synaptic changes observed here may be related to certain dynamic changes in receptive field properties that have been characterized in vivo.

Synaptic physiology of the flow of information in the cat's visual cortex in vivo

Each stage of the striate cortical circuit extracts novel information about the visual environment. We asked if this analytic process reflected laminar variations in synaptic physiology by making whole‐cell recording with dye‐filled electrodes from the cats visual cortex and thalamus; the stimuli were flashed spots. Thalamic afferents terminate in layer 4, which contains two types of cell, simple and complex, distinguished by the spatial structure of the receptive field. Previously, we had found that the postsynaptic and spike responses of simple cells reliably followed the time course of flash‐evoked thalamic activity. Here we report that complex cells in layer 4 (or cells intermediate between simple and complex) similarly reprised thalamic activity (response/trial, 99 ± 1.9 %; response duration 159 ± 57 ms; latency 25 ± 4 ms; average ± standard deviation; n= 7). Thus, all cells in layer 4 share a common synaptic physiology that allows secure integration of thalamic input. By contrast, at the second cortical stage (layer 2+3), where layer 4 directs its output, postsynaptic responses did not track simple patterns of antecedent activity. Typical responses to the static stimulus were intermittent and brief (response/trial, 31 ± 40 %; response duration 72 ± 60 ms, latency 39 ± 7 ms; n= 11). Only richer stimuli like those including motion evoked reliable responses. All told, the second level of cortical processing differs markedly from the first. At that later stage, ascending information seems strongly gated by connections between cortical neurons. Inputs must be combined in newly specified patterns to influence intracortical stages of processing.

Recoding of Sensory Information across the Retinothalamic Synapse

The neural code that represents the world is transformed at each stage of a sensory pathway. These transformations enable downstream neurons to recode information they receive from earlier stages. Using the retinothalamic synapse as a model system, we developed a theoretical framework to identify stimulus features that are inherited, gained, or lost across stages. Specifically, we observed that thalamic spikes encode novel, emergent, temporal features not conveyed by single retinal spikes. Furthermore, we found that thalamic spikes are not only more informative than retinal ones, as expected, but also more independent. Next, we asked how thalamic spikes gain sensitivity to the emergent features. Explicitly, we found that the emergent features are encoded by retinal spike pairs and then recoded into independent thalamic spikes. Finally, we built a model of synaptic transmission that reproduced our observations. Thus, our results established a link between synaptic mechanisms and the recoding of sensory information.