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

Abstract

18Stimulus-specific adaptation (SSA) is the reduction in responses to a common 19 stimulus that does not generalize, or only partially generalizes, to other stimuli. SSA 20 has been studied mainly with sounds that bear no behavioral meaning. We hypothesized 21 that the acquisition of behavioral meaning by a sound should modify the amount of 22 SSA evoked by that sound. To test this hypothesis, we used fear conditioning in rats, 23 using two word-like stimuli, derived from the English words "danger" and "safety", as 24 well as pure tones. One stimulus (CS+) was associated with a foot shock whereas the 25 other stimulus (CS-) was presented without a concomitant foot shock. We recorded 26 neural responses to the auditory stimuli using chronically implanted multi-electrode 27 arrays, recording responses telemetrically in freely moving animals before and after 28 conditioning. Consistent with our hypothesis, SSA changed in a way that depended on 29 the behavioral role of the sound: the contrast between standard and deviant responses 30 remained the same or decreased for CS+ stimuli but increased for CS-stimuli, showing 31 that SSA is shaped by experience. In most cases the sensory responses underlying these 32 changes in SSA increased following conditioning. Unexpectedly, the responses to CS+ 33 word-like stimuli showed a specific, substantial decrease, which we interpret as 34 evidence for substantial inhibitory plasticity. 59 discriminative fear conditioning paradigms): by the sa 60 stronger adaptation and therefore larger SSA following conditioning. 61It is now well established that learning modifies systematically the representation of 62 acoustic information in A1. Shifts of frequency tuning that favor behaviorally important 63 frequencies are a consistent finding across many types of training, reinforcement 64 motivation, and laboratories. Plasticity in A1 underlies at least some features of 65 auditory memory (20,21). Fear conditioning is an easy and robust way of modifying 66 animal behavior (22). When used with pure tones, the plastic changes that fear 67 conditioning induces in the auditory system are reasonably well-understood (23-25). 68We therefore used fear conditioning to explore the interaction of learning with SSA. 69 We used both pure tones and the word-like stimuli developed in Nelken et al. (19) for 70 discriminative fear conditioning, and measured the SSA evoked by these sounds before 71 and after conditioning. SSA indeed tended to decrease for the CS+ and increase for the 72 CS-sounds following conditioning. Unexpectedly, the patterns of changes in the neural 73 responses that led to these consequences was dependent on the acoustic structure of the 74 stimuli used during conditioning. Consistent with previous findings, conditioning with 75 pure tones increased neural responses to all stimuli. In contrast, conditioning with word-76 like stimuli led to a specific and surprisingly large decrease in the responses to the CS+ 77 stimulus. 78 Materials and Methods 79 Animals 80 The joint ethics...

Corticothalamic Projections Deliver Enhanced-Responses to Medial Geniculate Body as a Function of the Temporal Reliability of the Stimulus

“…7). 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 (Antunes et al, 2010;Richardson et al, 2013;Ayala et al, 2015;Duque & Malmierca, 2015;Cai et al, 2016a;Yaron et al, 2020). The increase in discharge rate with repetition is best explained by a buildup in the strength of the top-down/CT-mediated contribution to the MGB response (Fig.…”