Functional role of GABA in cat primary somatosensory cortex: shaping receptive fields of cortical neurons

Abstract

Extracellular recordings of 209 neurons were obtained with carbon fiber-containing multibarrel micropipettes. The cells were isolated in the primary somatosensory cortex of cats anesthetized with barbiturate and classified according to the nature of their response to natural stimuli, the nature of the surrounding multiunit responses to the same stimuli, the response to thalamic stimulation, and their depth in the cortex. To study factors controlling the excitability of somatosensory neurons, their receptive fields were examined in the presence of iontophoretically administered gamma-aminobutyric acid (GABA), glutamate, and bicuculline methiodide (BMI). Even when the neurons were depolarized to perithreshold levels with glutamate, or when local inhibitory influences mediated by GABA were antagonized by BMI, the apparent specificity for one class of afferent input was maintained. Neurons responding to stimulation of either cutaneous or deep receptors maintained their modality specificity, and neurons in cutaneous rapidly adapting regions never took on slowly adapting properties. When ejected at currents that did not elicit action potentials, glutamate lowered the threshold for activation by cutaneous stimuli but did not enlarge the receptive field. With larger ejecting currents, the neurons developed an on-going discharge, but even at these higher doses, glutamate did not produce an increase in the receptive-field size. Some neurons in regions of cortex exhibiting slowly adapting multiunit responses were relatively insensitive to glutamate. These cells required four to five times more glutamate to evoke discharges than did most neurons. Other cells, previously unresponsive to somatic stimuli, could be shown to possess distinct cutaneous receptive fields when either glutamate or BMI was ejected in their vicinity. Iontophoretically administered BMI altered the firing pattern of somatosensory neurons, causing them to discharge in bursts of 3-15 impulses. BMI enlarged the receptive-field size of neurons in regions displaying rapidly adapting multiunit background discharges but not in those regions with slowly adapting multiunit discharges. This differential effect of BMI, suggesting that GABA controls receptive-field size in rapidly adapting regions, also indicates that neurons in rapidly adapting regions differ pharmacologically from those in other submodality regions. In all cortical regions, BMI blocked the poststimulus inhibitory period that normally followed thalamic stimulation.(ABSTRACT TRUNCATED AT 400 WORDS)