Stimulus-specific adaptation to behaviorally-relevant sounds in awake rats

Abstract

Stimulus-specific adaptation (SSA) is the reduction in responses to a common stimulus that does not generalize, or only partially generalizes, to other stimuli. SSA has been studied mainly with sounds that bear no behavioral meaning. We hypothesized that the acquisition of behavioral meaning by a sound should modify the amount of SSA evoked by that sound. To test this hypothesis, we used fear conditioning in rats, using two word-like stimuli, derived from the English words "danger" and "safety", as well as pure tones. One stimulus (CS+) was associated with a foot shock whereas the other stimulus (CS-) was presented without a concomitant foot shock. We recorded neural responses to the auditory stimuli telemetrically, using chronically implanted multi-electrode arrays in freely moving animals before and after conditioning. Consistent with our hypothesis, SSA changed in a way that depended on the behavioral role of the sound: the contrast between standard and deviant responses remained the same or decreased for CS+ stimuli but increased for CS-stimuli, showing that SSA is shaped by experience. In most cases the sensory responses underlying these changes in SSA increased following conditioning. Unexpectedly, the responses to CS+ word-like stimuli showed a specific, large decrease, which we interpret as evidence for substantial inhibitory plasticity.

Corticothalamic projections deliver enhanced responses to medial geniculate body as a function of the temporal reliability of the stimulus

“…6). SSA studies using short tone-burst stimuli show significantly less adaptation across trials in awake animals, suggesting that top-down projections may reduce SSA in IC and MGB as suggested in the present study and previous studies (Antunes et al 2010;Richardson et al 2013;Ayala et al 2015;Duque & Malmierca, 2015;Cai et al 2016;Yaron et al 2020). The increase in discharge rate with repetition is best explained by a build-up in the strength of the top-down/CT-mediated contribution to the MGB response (Fig.…”

“…2016; Yaron et al . 2020). The increase in discharge rate with repetition is best explained by a build‐up in the strength of the top‐down/CT‐mediated contribution to the MGB response (Fig.…”

Prior unsupervised experience leads to long lasting effects in sensory gating during discrimination learning

“…In consequence of these changes, the contrast between standards and deviants (quantified as CSI) was larger after conditioning than before. This result is somewhat different than that in a previous report of plasticity of SSA (Yaron et al 2020), where the responses to pure tones used in conditioning and then tested as standards increased overall (rather than decreasing, as here). Potential reasons for this difference may be species differences (rats in Yaron et al 2020, mice in the current report), and the use of anesthesia (Yaron et al recorded in awake animals while the test recording in the current report were performed in anesthetized animals), but potentially the most important difference is the learning paradigm – Yaron et al used classical fear conditioning, while the current report used operant conditioning.…”

“…In addition to changes in sensory coding, learning may modify more abstract properties of cortical responses to sounds. For example, we have shown that fear conditioning modifies stimulus-specific adaptation (SSA; (Yaron et al 2020)). SSA is the decrease in neuronal responses to a repeated stimulus (adaptation) that does not, or only partially, generalize to other stimuli (Ulanovsky, Las, and Nelken 2003; Taaseh, Yaron, and Nelken 2011; Hershenhoren et al 2014; Carbajal and Malmierca 2018).…”

The generation of cortical novelty responses through inhibitory plasticity

“…The active amplification of novelty responses generated by our model is consistent with some experimental data (Taaseh et al, 2011;Hershenhoren et al, 2014;Hamm and Yuste, 2016;Harms et al, 2016), but see also (Vinken et al, 2017). Giving a behavioral meaning to a sound through fear conditioning has been shown to modify SSA (Yaron et al, 2020). Similarly, contrast adaptation has been shown to reverse when visual stimuli become behaviorally relevant (Keller et al, 2017).…”