GABA _B receptor-mediated, layer-specific synaptic plasticity reorganizes gamma-frequency neocortical response to stimulation

Abstract

Repeated presentations of sensory stimuli generate transient gamma-frequency (30-80 Hz) responses in neocortex that show plasticity in a task-dependent manner. Complex relationships between individual neuronal outputs and the mean, local field potential (population activity) accompany these changes, but little is known about the underlying mechanisms responsible. Here we show that transient stimulation of input layer 4 sufficient to generate gamma oscillations induced two different, lamina-specific plastic processes that correlated with lamina-specific changes in responses to further, repeated stimulation: Unit rates and recruitment showed overall enhancement in supragranular layers and suppression in infragranular layers associated with excitatory or inhibitory synaptic potentiation onto principal cells, respectively. Both synaptic processes were critically dependent on activation of GABA B receptors and, together, appeared to temporally segregate the cortical representation. These data suggest that adaptation to repetitive sensory input dramatically alters the spatiotemporal properties of the neocortical response in a manner that may both refine and minimize cortical output simultaneously.gamma rhythms | habituation | GABA B receptor | sensory processing | synaptic plasticity G amma-frequency (30-80 Hz) neuronal-population activity is a near-ubiquitous property of cortical responses to all modalities of sensory input (1). It is a feature of the temporal organization of outputs from neuronal ensembles and plays a critical role in intercortical communication and short-term memory (2). However, gamma-frequency responses are not stereotyped; they are powerfully influenced by neuromodulatory state and the nature of the cognitive task associated with sensory presentations. In particular they show plasticity, manifesting as changing local field potential power, frequency, spatial extent, and altered neuronal spike rates and spike-field coherences (3, 4). This plasticity is particularly overt on repeated presentation of familiar or novel discrete sensory stimuli (5-7).Understanding the processes underlying this plasticity is further complicated by the mechanistic inhomogeneity of brain rhythms within the gamma band. Both the lower (30-50 Hz) and higher (51-80 Hz) subbands are generated by fast spiking interneuronal recruitment into local circuit activity (8). However, in general they originate in different primary sensory cortical laminae and manifest in different cognitive states (9). In addition, although a repetition-related suppression of neuronal response has been most frequently described, notable examples have reported enhancements of both broadband gamma-frequency population activity (10) and discrete neuronal outputs (spikes) (11). Why enhancement or suppression is observed remains unclear. However, the direction of observed plasticity in the sensory gamma-frequency response can be influenced by task (12), stimuli (13), and the pattern of ongoing neuronal activity (5).Plasticity in the gamma-related cortical ...

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