Neurometabolic coupling differs for suppression within and beyond the classical receptive field in visual cortex

• Published in: The Journal of physiology Vol. 589; no. 13; pp. 3175 - 3190
• Main Authors: Li, Baowang, Freeman, Ralph D.
• Format: Journal Article
• Language: English
• Published: Oxford, UK Blackwell Publishing Ltd 01.07.2011; Wiley Subscription Services, Inc; Blackwell Science Inc
• Subjects: Animals; Cats; Cortex (visual); Female; Male; Metabolism; Metabolome - physiology; Neural Inhibition - physiology; Neural networks; Neurons; Neuroscience; Orientation; Oxygen consumption; Oxygen Consumption - physiology; Photic Stimulation - methods; Receptive field; Territory; Visual Cortex - metabolism; Visual Fields - physiology; Visual stimuli
• ISSN: 0022-3751; 1469-7793; 1469-7793
• DOI: 10.1113/jphysiol.2011.205039

Non‐technical summary  In visual cortex, underlying neural circuits process images by decoding responses of cells to specific stimuli. The transducer for this process is the receptive field, i.e. the territory which enables a single neuron to be highly selective for visual stimuli. Suppression effects within and outside the receptive field serve to shape the selectivity by modulation of neural firing. We show here that oxygen metabolism decreases or increases, respectively, for suppression within or outside the receptive field. The difference in activity‐induced oxygen demand between the two types of suppression helps clarify the function of associated neural circuits.   Neurons in visual cortex exhibit two major types of stimulus elicited suppression. One, cross‐orientation suppression, occurs within the classical receptive field (CRF) when an orthogonal grating is superposed on one at optimal orientation. The second, surround suppression, occurs when the size of an optimally oriented grating extends beyond the CRF. Previous proposals suggest that intracortical inhibition is responsible for surround suppression whereas feedforward processes may underlie cross‐orientation suppression. To gain more insight concerning these types of suppression, we have included measurements of metabolic function in addition to neural responses. We made co‐localized measurements of multiple unit neural activity and tissue oxygen concentrations in the striate cortex of anaesthetized cats while using visual stimuli to activate the two kinds of suppression. Results show that the amplitude of the initial negative oxygen response increases with stimulus size but neural responses decrease as size extends beyond the CRF. This shows that oxygen consumption increases with stimulus size regardless of reduced neural response. On the other hand, amplitudes of both the initial negative oxygen component and the neural responses are simultaneously attenuated by the orthogonal mask in cross‐orientation suppression. These different neurometabolic response patterns are consistent with suggestions that the two types of suppressive processes arise from different neural mechanisms.