Bertram R. Payne

Cortical feedback improves discrimination between figure and background by V1, V2 and V3 neurons.

A single visual stimulus activates neurons in many different cortical areas. A major challenge in cortical physiology is to understand how the neural activity in these numerous active zones leads to a unified percept of the visual scene. The anatomical basis for these interactions is the dense network of connections that link the visual areas. Within this network, feedforward connections transmit signals from lower-order areas such as V1 or V2 to higher-order areas. In addition, there is a dense web of feedback connections which, despite their anatomical prominence, remain functionally mysterious. Here we show, using reversible inactivation of a higher-order area (monkey area V5/MT), that feedback connections serve to amplify and focus activity of neurons in lower-order areas, and that they are important in the differentiation of figure from ground, particularly in the case of stimuli of low visibility. More specifically, we show that feedback connections facilitate responses to objects moving within the classical receptive field; enhance suppression evoked by background stimuli in the surrounding region; and have the strongest effects for stimuli of low salience.

The cryoloop: an adaptable reversible cooling deactivation method for behavioral or electrophysiological assessment of neural function.

We describe a very adaptable reversible inactivation technique for the behavioral or electrophysiological analysis of neural circuits. The cryoloop device can be permanently implanted or topically applied in an acute preparation to apply cold to discrete surface regions of the central nervous system (e.g. cerebral cortex or midbrain). The cryoloop consists of a custom shaped, stainless steel, hypodermic tubing and cooling is effected by passing chilled methanol through the lumen of the tubing. Cryoloop temperature is monitored by a microthermocouple attached to the union of the loop, and can be maintained within +/- 1 degrees C of a desired temperature. In chronic preparations, implanted cryoloops have been maintained in cats and monkeys for periods in excess of 2 years. After this period there are no structural, metabolic of functional changes in the deactivated tissue, and full reversibility of cooling-induced effects is maintained. Operation of multiple cryoprobes provides great flexibility of experimental protocols, permits double and triple functional dissociations to be made, and strengthens experimental design considerably.

Removal of two halves restores the whole: Reversal of visual hemineglect during bilateral cortical or collicular inactivation in the cat

The purpose of the present study was to compare visual orienting behavior in the adult cat during (1) unilateral and bilateral cooling deactivation of posterior-middle suprasylvian (pMS) sulcal cortex, and (2) unilateral and bilateral deactivation of the superior colliculus. As expected, unilateral cooling deactivation of either pMS cortex or the superior colliculus resulted in a profound visual neglect of the contracooled hemifield. The addition of cooling the homotopic region in the opposite hemisphere largely reversed this deficit and restored visual orienting into the previously neglected hemifield. These results show that (1) pMS cortex and the superior colliculus are essential for normal detection and orienting to visual targets, and (2) unilateral visual neglect results from an imbalance of activities in the two hemispheres induced at either cortical or subcortical levels. These conclusions have implications for understanding neural bases of visual hemineglect following unilateral lesions in humans.

Impact of repetitive transcranial magnetic stimulation of the parietal cortex on metabolic brain activity: a 14C-2DG tracing study in the cat

Transcranial magnetic stimulation (TMS) is increasingly utilized in clinical neurology and neuroscience. However, detailed knowledge of the impact and specificity of the effects of TMS on brain activity remains unresolved. We have used 14C-labeled deoxyglucose (14C-2DG) mapping during repetitive TMS (rTMS) of the posterior and inferior parietal cortex in anesthetized cats to study, with exquisite spatial resolution, the local and distant effects of rTMS on brain activity. High-frequency rTMS decreases metabolic activity at the primary site of stimulation with respect to homologue areas in the unstimulated hemisphere. In addition, rTMS induces specific distant effects on cortical and subcortical regions known to receive substantial efferent projections from the stimulated cortex. The magnitude of this distal impact is correlated with the strength of the anatomical projections. Thus, in the anesthetized animal, the impact of rTMS is upon a distributed network of structures connected to the primary site of application.

The role of feedback in shaping neural representations in cat visual cortex

In the primary visual cortex, neurons with similar response preferences are grouped into domains forming continuous maps of stimulus orientation and direction of movement. These properties are widely believed to result from the combination of ascending and lateral interactions in the visual system. We have tested this view by examining the influence of deactivating feedback signals descending from the visuoparietal cortex on the emergence of these response properties and representations in cat area 18. We thermally deactivated the dominant motion-processing region of the visuoparietal cortex and used optical and electrophysiological methods to assay neural activity evoked in area 18 by stimulation with moving gratings and fields of coherently moving randomly distributed dots. Feedback deactivation decreased signal strength in both orientation and direction maps and virtually abolished the global layout of direction maps, whereas the basic structure of the orientation maps was preserved. These findings could be accounted for by a selective silencing of highly direction-selective neurons and by the redirection of preferences of less selective neurons. Our data suggest that signals fed back from the visuoparietal cortex strongly contribute to the emergence of direction selectivity in early visual areas. Thus we propose that higher cortical areas have significant influence over fundamental neuronal properties as they emerge in lower areas.

Thalamic and cortical projections to middle suprasylvian cortex of cats: constancy and variation

Abstract We investigated the constancy and variability in the numbers of thalamic and cortical neurons projecting to cat middle suprasylvian (MS) visual cortex. Retrograde pathway tracers were injected at a single anatomically and physiologically defined locus in MS cortex. Counts of labeled neurons showed that the visual thalamic projections to MS cortex consistently arose from a fixed set of nuclei in relatively constant proportions. In contrast, counts of cortical neurons revealed that transcortical inputs to MS cortex were much more variable. This differential variability may be linked to the developmental program, which affords greater influence of experiential factors on cortical pathway development than on thalamocortical pathway development. These results have implications for the development of models of cerebral connectivity that include measures of pathway variability.

Role of the superior colliculus in analyses of space: Superficial and intermediate layer contributions to visual orienting, auditory orienting, and visuospatial discriminations during unilateral and bilateral deactivations

The superior colliculus (SC) has been implicated in spatial analyses of the environment, although few behavioral studies have explicitly tested this role. To test its imputed role in spatial analyses, we used a battery of four spatial tasks combined with unilateral and bilateral cooling deactivation of the upper and intermediate layers of the superior colliculus. We tested the abilities of cats to orient to three different stimuli: (1) moving visual, (2) stationary visual, (3) stationary white‐noise aural. Furthermore, we tested the ability of the cats to discriminate the relative spatial position of a landmark. Unilateral cooling deactivation of the superficial layers of the SC induced a profound neglect of both moving and stationary visual stimuli presented in, and landmark objects located within, the contralateral hemifield. However, responses to auditory stimuli were unimpaired. Unilateral cooling deactivation of both the superficial and intermediate layers induced a profound contralateral neglect of the auditory stimulus. Additional and equivalent deactivation of the opposite SC largely restored orienting to either moving visual or auditory stimuli, and restored landmark position reporting to normal levels. However, during bilateral SC deactivation, orienting to the static visual stimulus was abolished throughout the entire visual field. Overall, unilateral SC deactivation results show that the upper and intermediate layers of the SC contribute in different ways to guiding behavioral responses to visual and auditory stimuli cues. Finally, bilateral superior colliculus deactivations reveal that other structures are sufficient to support spatial analyses and guide visual behaviors in the absence of neural operations in the superior colliculus, but only under certain circumstances. J. Comp. Neurol. 441:44–57, 2001.

Reconstructing functional systems after lesions of cerebral cortex

The young brain is enormously resilient to early injury. This resiliency contrasts with the severe and permanent impairments that frequently accompany equivalent damage to the mature cerebrum. For example, damage to Brocas area renders the patient unable to speak, but equivalent damage early in life does not have such devastating effects. Here we review the history of the study of early lesion-induced plasticity, and delineate the features of the developing brain that permit it to overcome the effects of early cerebral lesions. We also speculate on future avenues of investigation that should help us to comprehend how young brains are naturally rebuilt after early lesions.

Evidence for greater sight in blindsight following damage of primary visual cortex early in life

This review compares the behavioral, physiological and anatomical repercussions of lesions of primary visual cortex incurred by developing and mature humans, monkey and cats. Comparison of the data on the repercussions following lesions incurred earlier or later in life suggests that earlier, but not later, damage unmasks a latent flexibility of the brain to compensate partially for functions normally attributed to the damaged cortex. The compensations are best documented in the cat and they can be linked to system-wide repercussions that include selected pathway expansions and neuron degenerations, and functional adjustments in neuronal activity. Even though evidence from humans and monkeys is extremely limited, it is argued on the basis of known repercussions and similarity of visual system organization and developmental sequence, that broadly equivalent repercussions most likely occur in humans and monkeys following early lesions of primary visual cortex. The extant data suggest potentially useful directions for future investigations on functional anatomical aspects of visual capacities spared in human patients and monkeys following early damage of primary visual cortex. Such research is likely to have a substantial impact on increasing our understanding of the repercussions that result from damage elsewhere in the developing cerebral cortex and it is likely to contribute to our understanding of the remarkable ability of the human brain to adapt to insults.

Complex transcallosal interactions in visual cortex.

Reversible inactivation by cooling of the transcallosal projecting neurons in areas 17 and 18 of one hemisphere bring about complex changes in the spontaneous and evoked activity of neurons in the callosal receiving zone of the opposite hemisphere. These changes include increases and decreases in evoked and spontaneous activities. Overall, 90% of neurons in layers II and III, 50% in layer IV, and 100% in layers V and VI were affected by the block of transcallosal input. The complexity of the changes was greatest in layers II and III, which are the major callosal recipient layers. The results indicate that many excitatory and inhibitory circuits are under the direct control of transcallosal fibers in the normally functioning brain.