Towards a Theory of the Laminar Architecture of Cerebral Cortex: Computational Clues from the Visual System

One of the most exciting and open research frontiers in neuroscience is that of seeking to understand the functional roles of the layers of cerebral cortex. New experimental techniques for probing the laminar circuitry of cortex have recently been developed, opening up novel opportunities for investigating ho1v its six-layered architecture contributes to perception and cognition. The task of trying to interpret this complex structure can be facilitated by theoretical analyses of the types of computations that cortex is carrying out, and of how these might be implemented in specific cortical circuits. We have recently developed a detailed neural model of how the parvocellular stream of the visual cortex utilizes its feedforward, feedback, and horizontal interactions for purposes of visual filtering, attention, and perceptual grouping. This model, called LAMINART, shows how these perceptual processes relate to the mechanisms which ensure stable development of cortical circuits in the infant, and to the continued stability of learning in the adult. The present article reviews this laminar theory of visual cortex, considers how it may be generalized towards a more comprehensive theory that encompasses other cortical areas and cognitive processes, and shows how its laminar framework generates a variety of testable predictions.Defense Advanced Research Projects Agency and the Office of Naval Research (N00014-95-0409); National Science Foundation (IRI 94-01659); Office of Naval Research (N00014-92-1-1309, N00014-95-1-0657

Modeling direction selectivity of simple cells in striate visual cortex within the framework of the canonical microcircuit

Nearly all models of direction selectivity (DS) in visual cortex are based on feedforward connection schemes, where geniculate input provides all excitatory synaptic input to both pyramidal and inhibitory neurons. Feedforward inhibition then suppresses feedforward excitation for nonoptimal stimuli. Anatomically, however, the majority of asymmetric, excitatory, synaptic contacts onto cortical cells is provided by other cortical neurons, as embodied in the Canonical Microcircuit of Douglas and Martin (1991). In this view, weak geniculate input is strongly amplified in the preferred direction by the action of intracortical excitatory connections, while in the null direction inhibition reduces geniculate-induced excitation. We investigate analytically and through biologically realistic computer simulations the functioning of a cortical network based on massive excitatory, cortico-cortical feedback. The behavior of this network is compared to physiological data as well as to the behavior of a purely feedforward model of DS based on nonlagged input. Our model explains a number of puzzling features of direction selective simple cells, including the small somatic input conductance changes that have been measured experimentally during stimulation in the null direction, and the persistence of DS while fully blocking inhibition in a single cell. Although the operation at the heart of our network is amplification, the network passes the linearity test of (Jagadeesh et al., 1993). We make specific predictions concerning the effect of selective blockade of cortical inhibition on the velocity-response curve

Anatomy and Physiology of Macaque Visual Cortical Areas V1, V2, and V5/MT : Bases for Biologically Realistic Models

The cerebral cortex of primates encompasses multiple anatomically and physiologically distinct areas processing visual information. Areas V1, V2, and VS/MT are conserved across mammals and are central for visual behavior. To facilitate the generation of biologically accurate computational models of primate early visual processing, here we provide an overview of over 350 published studies of these three areas in the genus Macaca, whose visual system provides the closest model for human vision. The literature reports 14 anatomical connection types from the lateral geniculate nucleus of the thalamus to V1 having distinct layers of origin or termination, and 194 connection types between V1, V2, and VS, forming multiple parallel and interacting visual processing streams. Moreover, within V1, there are reports of 286 and 120 types of intrinsic excitatory and inhibitory connections, respectively. Physiologically, tuning of neuronal responses to 11 types of visual stimulus parameters has been consistently reported. Overall, the optimal spatial frequency (SF) of constituent neurons decreases with cortical hierarchy. Moreover, VS neurons are distinct from neurons in other areas for their higher direction selectivity, higher contrast sensitivity, higher temporal frequency tuning, and wider SF bandwidth. We also discuss currently unavailable data that could be useful for biologically accurate models.Peer reviewe

Processing of transient stimuli by the visual system of the rat

While three decades of intensive cortical electrophysiology using a variety of sustained visual stimuli has made a significant contribution to many aspects of visual function, it has not supported the existence of intracortical circuit operations in cortical processing. This study investigated cortical processing by a comparison of the response of primary visual cortical neurones to transient electrical and strobe-flash stimulation. Experiments were performed on 74 anaesthetised Long Evans rats. Standard stereotaxic and extracellular electrophysiological techniques were employed. Continuous (on-line) raster plots and peri-stimulus time histograms (PSTHs) of the extracellular spikes from 81 visual cortical and 55 lateral geniculate nucleus (LGN) neurones were compiled. The strobe-flash stimuli (0.05 ms) were applied to the contralateral eye while the monopolar or bipolar electrical stimuli (0.2 ms, 80-400 μA) were applied to the ipsilateral LGN. 60 of the 81 (74%) tested cortical units were found to be responsive to visual stimuli. A distinct and consistent difference in the cortical response to the two types of transient stimuli was found: (a) Electrical stimulation evoked a prolonged period (197 ± 61 ms) of inhibition in all cortical neurones tested (n=20). This was the case even in those cortical units that were completely unresponsive to visual stimulation. The protracted inhibition was usually followed by a 100-200 ms phase of rebound excitation. (b) Flash stimulation evoked a prominent excitatory discharge (5-30 ms duration) after a latency of 30-60 ms from the onset of the stimulus (n = 59). This was followed by either moderate inhibition or return to a firing rate similar to control activity, for a maximum of 40 ms. Thereafter, cortical neurones showed a sustained increased level of activity with superimposed secondary excitatory phases. The duration of this late re-excitatory phase was 200-300 ms. In 17 of 20 (85%) tested units, the temporal profile of the cortical response to flash stimulation was modulated by small changes in the level of background illumination. In 16 of the 17 units, this sensitivity was reflected primarily as an emergence of a brief secondary inhibitory phase at the lowest level of background illumination (0 lux). Only 1 of the 17 cortical units displayed a flash-evoked primary inhibitory phase at O lux. We explored the possibility that neurones in the lateral geniculate nucleus (LGN) of the thalamus were responsible for the late phase of cortical reexcitation. 49 of the 55 (89%) LGN neurones could be classified as either of the "ON type" i.e. excited by visual stimuli, or the "OFF type" i.e. inhibited by visual stimuli. The response of ON-like LGN neurones to strobe-flash stimulation of the contralateral eye was characterised by a primary excitatory or early discharge (ED) phase after a latency of 25-40 ms. Thereafter, a 200- 400 ms period of inhibition was observed. In 57% of the sample, a rebound excitatory or late discharge (LD) phase completed the response. OFF-like LGN neurones were inhibited by the strobe-flash stimuli after a latency of 30- 35 ms. This flash-evoked inhibition was maintained for 200-400 ms. The sensitivity of the flash-evoked LGN response to the level of background illumination was tested in 11 ON-like and 10 OFF-like neurones. No sustained secondary excitatory events, as observed in visual cortical neurones, were found in any of the ON- and OFF-like LGN neurones, irrespective of the level of background illumination. In conclusion, the data show that the late re-excitatory phase evoked in cortical neurones upon strobe-flash stimulation, is not due to sustained LGN (thalamic) input. Rather, it suggests that these re-excitatory phases are due to intracortical processing of the transient stimuli. These findings emphasize the independent role of the cortex in computing the response to visual stimuli, and cast doubt on traditional theories that have emphasised the role of the thalamus in shaping cortical responses. The difference in the flash and electrically evoked cortical response suggests that even though substantial inhibition is available to the cortex, only a small fraction of this inhibitory capacity is utilised during natural stimulation