Intrinsic Mechanisms for Adaptive Gain Rescaling in Barrel Cortex

Abstract

Barrel cortex neuronal responses adapt to changes in the statistics of complex whisker stimuli. This form of adaptation involves an adjustment in the input-output tuning functions of the neurons, such that their gain rescales depending on the range of the current stimulus distribution. Similar phenomena have been observed in other sensory systems, suggesting that adaptive adjustment of responses to ongoing stimulus statistics is an important principle of sensory function. In other systems, adaptation and gain rescaling can depend on intrinsic properties; however, in barrel cortex, whether intrinsic mechanisms can contribute to adaptation to stimulus statistics is unknown. To examine this, we performed whole-cell patch-clamp recordings of pyramidal cells in acute slices while injecting stochastic current stimuli. We induced changes in statistical context by switching across stimulus distributions. The firing rates of neurons adapted in response to changes in stimulus statistics. Adaptation depended on the form of the changes in stimulus distribution: in vivo-like adaptation occurred only for rectified stimuli that maintained neurons in a persistent state of net depolarization. Under these conditions, neurons rescaled the gain of their input-output functions according to the scale of the stimulus distribution, as observed in vivo. This stimulus-specific adaptation was caused by intrinsic properties and correlated strongly with the amplitude of calciumdependent slow afterhyperpolarizations. Our results suggest that widely expressed intrinsic mechanisms participate in barrel cortex adaptation but that their recruitment is highly stimulus specific.

Multiple Timescale Encoding of Slowly Varying Whisker Stimulus Envelope in Cortical and Thalamic NeuronsIn Vivo

“…The adaptation we measured in cortical neurons is likely attributable to a combination of intrinsic mechanisms (Díaz-Quesada and Maravall, 2008;Lundstrom et al, 2008) and thalamocortical and intracortical synaptic depression (Katz et al, 2006). The reduction in cortical firing rate in response to repetitive whisker deflections at a given frequency is in part attributable to depression at thalamocortical synapses (Castro-Alamancos and Oldford, 2002;Chung et al, 2002;Khatri et al, 2004;Petersen et al, 2009).…”

Emergence of Adaptive Computation by Single Neurons in the Developing Cortex

“…As intrinsic properties shift with expression of channels with specific functional roles (Connors and Gutnick, 1990;Maravall et al, 2007;Díaz-Quesada and Maravall, 2008), gain-scaling behavior might be supported by a different mechanism, such as the slow AHP current observed in the adult barrel cortex (Díaz-Quesada and Maravall, 2008).…”

“…In retinal ganglion cells, gain control has been attributed to slow sodium inactivation leading to a -dependent build-up of inactivation (Kim and Rieke, 2001). In adult barrel cortex neurons, contributions to gain scaling have been associated with a calcium-activated potassium conductance underlying slow afterspike hyperpolarization (Díaz-Quesada and Maravall, 2008). In these cases, the effect was attributed to a relatively slow-timescale activity-dependent current that reduced threshold in the presence of increased neuronal activity.…”

Sensory Input Drives Multiple Intracellular Information Streams in Somatosensory Cortex

“…Indeed, neurons integrating their synaptic inputs can readjust their sensitivity, and hence their resolution, via a multitude of adaptive mechanisms: these can render neurons preferentially sensitive to, for example, signals in particular frequency ranges (Azouz andGray, 1999, 2003;Azouz, 2005;Léger et al, 2005;Prescott and De Koninck, 2005;Higgs et al, 2006;Díaz-Quesada and Maravall, 2008) (Fig. 4 A, green scale at right).…”

“…Is this operation biologically plausible? Substantial evidence suggests that the multiplexed information in different frequency bands is likely accessible to neurons through their mechanisms for synaptic integration, for example, through changes in integration time constant or spike threshold (Azouz andGray, 1999, 2003;Azouz, 2005;Léger et al, 2005;Prescott and De Koninck, 2005;Higgs et al, 2006;Díaz-Quesada et al, 2008). Similarly, neurons may be sensitive to a specific feature (such as phase or amplitude) within a frequency channel.…”