Excitotoxic lesions of the superior colliculus preferentially impact multisensory neurons and multisensory integration

• Published in: Experimental brain research Vol. 179; no. 2; pp. 325 - 338
• Main Authors: BURNETT, Luke R, STEIN, Barry E, PERRAULT, Thomas J, WALLACE, Mark T
• Format: Journal Article
• Language: English
• Published: Berlin Springer 01.05.2007; Springer Nature B.V
• Subjects: Animals; Behavior; Biological and medical sciences; Brain Mapping; Cats; Cerebral Cortex - physiology; Electrodes, Implanted; Electrophysiology; Excitatory Amino Acid Agonists - toxicity; Excitotoxicity; Eye and associated structures. Visual pathways and centers. Vision; Functional Laterality - physiology; Fundamental and applied biological sciences. Psychology; Immunohistochemistry; Laboratory animals; Lesions; Motor control and motor pathways. Reflexes. Control centers of vegetative functions. Vestibular system and equilibration; N-Methylaspartate - toxicity; Neuronal Plasticity - drug effects; Neuronal Plasticity - physiology; Neurons; Neurons, Afferent - drug effects; Neurons, Afferent - pathology; Neurons, Afferent - physiology; Neurosciences; Orientation; Photic Stimulation; Physiology; Sensory integration; Superior Colliculi - drug effects; Superior Colliculi - pathology; Superior Colliculi - physiology; Superior colliculus; Vertebrates: nervous system and sense organs; United States > US; Fissipedia; Carnivora; Receptive field; Central nervous system; Multisensory integration; Orientation; Cross-modal; Colliculus superior; Encephalon; Eye; Visual system; Vertebrata; Mammalia; Polysensorial neuron; Visual pathway; Cell death; Cat; Plasticity; NMDA· Plasticity
• ISSN: 0014-4819; 1432-1106
• DOI: 10.1007/s00221-006-0789-8

The superior colliculus (SC) plays an important role in integrating visual, auditory and somatosensory information, and in guiding the orientation of the eyes, ears and head. Previously we have shown that cats with unilateral SC lesions showed a preferential loss of multisensory orientation behaviors for stimuli contralateral to the lesion. Surprisingly, this behavioral loss was seen even under circumstances where the SC lesion was far from complete. To assess the physiological changes induced by these lesions, we employed single unit electrophysiological methods to record from individual neurons in both the intact and damaged SC following behavioral testing in two animals. In the damaged SC of these animals, multisensory neurons were preferentially reduced in incidence, comprising less than 25% of the sensory-responsive population (as compared with 49% on the control side). In those multisensory neurons that remained following the lesion, receptive fields were nearly twofold larger, and less than 25% showed normal patterns of multisensory integration, with those that did being found in areas outside of the lesion. These results strongly suggest that the multisensory behavioral deficits seen following SC lesions are the combined result of a loss of multisensory neurons and a loss of multisensory integration in those neurons that remain.