Charles D. Gilbert

Functional architecture of cortex revealed by optical imaging of intrinsic signals.

Optical imaging of cortical activity offers several advantages over conventional electrophysiological and anatomical techniques. One can map a relatively large region, obtain successive maps to different stimuli in the same cortical area and follow variations in response over time. In the intact mammalian brain this imaging has been accomplished with the aid of voltage sensitive dyes1–5. However, it has been known for many years that some intrinsic changes in the optical properties of the tissue are dependent on electrical or metabolic activity6–13. Here we show that these changes can be used to study the functional architecture of cortex. Optical maps of whisker barrels in the rat and the orientation columns in the cat visual cortex, obtained by reflection measurements of the intrinsic signal, were confirmed with voltage sensitive dyes or by electrophysiological recordings. In addition, we describe an intrinsic signal originating from small arteries which can be used to investigate the communication between local neuronal activity and the microvasculature. One advantage of the method is that it is non-invasive and does not require dyes, a clear benefit for clinical applications.

Morphology and intracortical projections of functionally characterised neurones in the cat visual cortex.

The neuronal structure and connectivity underlying receptive field organisation of cells in the cat visual cortex have been investigated. Intracellular recordings were made using a micropipette filled with a histochemical marker, which was injected into the cells after their receptive fields had been characterised. This allowed visualisation of the dendritic and axonal arborisations of functionally identified neurones

Improvement in Visual Sensitivity by Changes in Local Context: Parallel Studies in Human Observers and in V1 of Alert Monkeys

To explore the role of primary visual cortex in contour integration, we measured the contextual sensitivity of human contrast thresholds and of superficial layer complex cells in monkey V1. An observers contrast detection was 40% improved by a second suprathreshold bar; the effect was decreased as the two bars were separated along their axis of orientation, were displaced from colinearity, and had their relative orientation changed. Recordings from V1 showed that 42% of complex cells demonstrated facilitation for a second bar outside their classical receptive fields with a similar dependency on relative location and orientation. Both effects were eliminated by an orthogonal line between the two iso-oriented lines. Multiple randomly placed and oriented lines in the receptive field surround often caused a reduction in a cells response to an optimally oriented stimulus, but this inhibition could be eliminated by changing the orientation of a few of these elements to colinearity with the centrally located target.

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.

The Neural Basis of Perceptual Learning

Perceptual learning is a lifelong process. We begin by encoding information about the basic structure of the natural world and continue to assimilate information about specific patterns with which we become familiar. The specificity of the learning suggests that all areas of the cerebral cortex are plastic and can represent various aspects of learned information. The neural substrate of perceptual learning relates to the nature of the neural code itself, including changes in cortical maps, in the temporal characteristics of neuronal responses, and in modulation of contextual influences. Top-down control of these representations suggests that learning involves an interaction between multiple cortical areas.

Brain States: Top-Down Influences in Sensory Processing

All cortical and thalamic levels of sensory processing are subject to powerful top-down influences, the shaping of lower-level processes by more complex information. New findings on the diversity of top-down interactions show that cortical areas function as adaptive processors, being subject to attention, expectation, and perceptual task. Brain states are determined by the interactions between multiple cortical areas and the modulation of intrinsic circuits by feedback connections. In perceptual learning, both the encoding and recall of learned information involves a selection of the appropriate inputs that convey information about the stimulus being discriminated. Disruption of this interaction may lead to behavioral disorders, including schizophrenia.

Horizontal Integration and Cortical Dynamics

We have discussed several results that lead to a view that cells in the visual system are endowed with dynamic properties, influenced by context, expectation, and long-term modifications of the cortical network. These observations will be important for understanding how neuronal ensembles produce a system that perceives, remembers, and adapts to injury. The advantage to being able to observe changes at early stages in a sensory pathway is that one may be able to understand the way in which neuronal ensembles encode and represent images at the level of their receptive field properties, of cortical topographies, and of the patterns of connections between cells participating in a network.

Laminar patterns of geniculocortical projection in the cat

The cortical afferents from individual laminae of the dorsal lateral geniculate nucleus (LGN) were studied using both light and electron microscope autoradiography. In area 17, the A geniculate laminae (A and A1) had two main bands of projection, one extending from the bottom of IVc to the deepest cells in layer III, and one in layer VI. The C geniculate laminae projected in two dense bands to the upper and lower borders of layer IV, thus bracketing the A laminae projection, though with some overlap. In addition, the C laminae projected to the superficial half of layer I, which the A laminae did not. Conversely, while the A laminae projected to layer VI, the C laminae did not. The two sets of laminae also showed differences in the areas to which they projected. The A geniculate laminae projected to areas 17 and 18, whereas the C geniculate laminae had a more extensive projection, including areas 17, 18, 19 and other areas on the suprasylvian gyrus. The laminar organization of the projection to area 18 was similar to that found in area 17. At the electron microscopic level the geniculate terminals were found to make Grays type 1 synapses, for the most part onto dendritic spines. Labeled terminals were found in all the projection bands seen in the light microscope. The implications of these findings on the connectivity of cells in layer IV are discussed. The presence of labeled terminals in layer VI, which contains the cells of origin of the corticogeniculate pathway, suggests that the recurrent loop to the LGN is mediated monosynaptically. Finally, the afferents from each geniculate lamina were found to be segregated into patches, about 500 mum wide, which probably form the anatomical basis for ocular dominance columns.

Attention Modulates Contextual Influences in the Primary Visual Cortex of Alert Monkeys

The response properties of cells in the primary visual cortex (V1) were measured while the animals directed their attention either to the position of the neurons receptive field (RF), to a position away from the RF (focal attention), or to four locations in the visual field (distributed attention). Over the population, varying attentional state had no significant effect on the response to an isolated stimulus within the RF but had a large influence on the facilitatory effects of contextual lines. We propose that the attentional modulation of contextual effects represents a gating of long range horizontal connections within area V1 by feedback connections to V1 and that this gating provides a mechanism for shaping responses under attention to stimulus configuration.

Perceptual learning and top-down influences in primary visual cortex.

Neuronal responses at early stages in visual cortical processing, including those in primary visual cortex (V1), are subject to the influences of visual context, experience and attention. Here we show that for monkeys trained in a shape discrimination task, V1 neurons took on novel functional properties related to the attributes of the trained shapes. Furthermore, these properties depended on the perceptual task being performed; neurons responded very differently to an identical visual stimulus under different visual discrimination tasks. These top-down influences were seen from the very beginning and throughout the entire time course of the neural responses. Information theoretic analysis showed that neurons carried more information about a stimulus attribute when the animals were performing a task related to that attribute. Our findings suggest that the output from V1 reflects both sensory and behavioral context.