Nonmonotonic Synaptic Excitation and Imbalanced Inhibition Underlying Cortical Intensity Tuning

Abstract

Intensity-tuned neurons, characterized by their nonmonotonic response-level function, may play important roles in the encoding of sound intensity-related information. The synaptic mechanisms underlying intensity tuning remain unclear. Here, in vivo whole-cell recordings in rat auditory cortex revealed that intensity-tuned neurons, mostly clustered in a posterior zone, receive imbalanced tone-evoked excitatory and inhibitory synaptic inputs. Excitatory inputs exhibit nonmonotonic intensity tuning, whereas with tone intensity increments, the temporally delayed inhibitory inputs increase monotonically in strength. In addition, this delay reduces with the increase of intensity, resulting in an enhanced suppression of excitation at high intensities and a significant sharpening of intensity tuning. In contrast, non-intensity-tuned neurons exhibit covaried excitatory and inhibitory inputs, and the relative time interval between them is stable with intensity increments, resulting in monotonic response-level function. Thus, cortical intensity tuning is primarily determined by excitatory inputs and shaped by cortical inhibition through a dynamic control of excitatory and inhibitory timing.

Shift in the Balance between Excitation and Inhibition during Sensory Adaptation of S1 Neurons

“…In agreement with others (Wehr and Zador, 2003;Tan et al, 2004;Wehr and Zador, 2005;Wilent and Contreras, 2005;Higley and Contreras, 2006;Wu et al, 2006), we observed that sensory stimulation evokes a stereotypic activation of excitation that was closely followed by a strong inhibition. The stronger inhibitory conductance, relative to the excitatory input, may reflect the larger unitary excitatory post synaptic current (EPSC) of impinging thalamic inputs on inhibitory neurons compared with those that impinge on excitatory cells (Porter et al, 2001;Cruikshank et al, 2007) and the robust firing of fast-spiking neurons during whisker stimulation (Swadlow and Gusev, 2000;Bruno and Simons, 2002).…”

Control of neuronal firing by dynamic parallel fiber feedback:implications for electrosensory reafference suppression

“…The resulting non-monotonic response in pyramidal neuron firing is similar to that described in other studies, involving both experimental and modeling contexts (e.g. Wu et al, 2006;Tan et al, 2007;Mikula and Niebur, 2003;Kuhn et al, 2004;de la Rocha and Parga, 2005). However, the underlying mechanisms vary.…”

Altered Neural Responses to Sounds in Primate Primary Auditory Cortex during Slow-Wave Sleep

“…An important property in sharpening neural tuning (Wu et al, 2008;Sadagopan and Wang, 2010) and expanding dynamic range (Wu et al, 2006;Tan et al, 2007) is inhibition. Here, we isolated events where firing rate was suppressed below spontaneous firing rate (see Materials and Methods) as a possible window into inhibitory processes ( Fig.…”

“…This hypothesis would be easy to test either directly through intracellular recordings or indirectly by observing signatures of inhibition, such as its noted presence at high sound levels (Wu et al, 2006;Tan et al, 2007;Sadagopan and Wang, 2010) or its influence on correlated network activity (Wang, 2010). We did not test sound levels beyond 70 dB SPL except in a few cases to limit awakening the animals.…”