Stimulus-specific adaptation (SSA) is the specific decrease in the response to a frequent (‘standard’) stimulus, which does not generalize, or generalizes only partially, to another, rare stimulus (‘deviant’). Stimulus-specific adaptation could result simply from the depression of the responses to the standard. Alternatively, there may be an increase in the responses to the deviant stimulus due to the violation of expectations set by the standard, indicating the presence of true deviance detection. We studied SSA in the auditory cortex of halothane-anesthetized rats, recording local field potentials and multi-unit activity. We tested the responses to pure tones of one frequency when embedded in sequences that differed from each other in the frequency and probability of the tones composing them. The responses to tones of the same frequency were larger when deviant than when standard, even with inter-stimulus time intervals of almost 2 seconds. Thus, SSA is present and strong in rat auditory cortex. SSA was present even when the frequency difference between deviants and standards was as small as 10%, substantially smaller than the typical width of cortical tuning curves, revealing hyper-resolution in frequency. Strong responses were evoked also by a rare tone presented by itself, and by rare tones presented as part of a sequence of many widely spaced frequencies. On the other hand, when presented within a sequence of narrowly spaced frequencies, the responses to a tone, even when rare, were smaller. A model of SSA that included only adaptation of the responses in narrow frequency channels predicted responses to the deviants that were substantially smaller than the observed ones. Thus, the response to a deviant is at least partially due to the change it represents relative to the regularity set by the standard tone, indicating the presence of true deviance detection in rat auditory cortex.
Neurons in auditory cortex are sensitive to the probability of stimuli: responses to rare stimuli tend to be stronger than responses to common ones. Here, intra- and extracellular recordings from the auditory cortex of halothane-anesthetized rats revealed the existence of a finer sensitivity to the structure of sound sequences. Using oddball sequences in which the order of stimulus presentations is periodic, we found that tones in periodic sequences evoked smaller responses than the same tones in random sequences. Significant reduction in the responses to the common tones in periodic relative to random sequences occurred even when these tones consisted of 95% of the stimuli in the sequence. The reduction in responses paralleled the complexity of the sound sequences and could not be explained by short-term effects of clusters of deviants on succeeding standards. We conclude that neurons in auditory cortex are sensitive to the detailed structure of sound sequences over timescales of minutes.
Detecting rare and surprising events is a useful strategy for sensory -systems. In the human auditory system, deviance detection is indexed by an important component of the auditory event-related potentials, the mismatch negativity (MMN). Responses of single neurons in the inferior colliculus, medial geniculate body, and auditory cortex of mammals (cats, rats, and mice) show responses that share some properties with MMN: they are evoked by rare events, are preattentive (in as much as they occur in anesthetized animals), and, at least at the level of primary auditory cortex, cannot be accounted for by simple fatigue of the incoming sensory information. Here we extend these results to deviations beyond tone frequency. Recording in rat primary auditory cortex and using oddball sequences consisting of two frozen tokens of broadband noise samples, we found differences between the responses to the same token when used as the common and when used as the deviant, showing an exquisite sensitivity to the small differences between two spectro-temporally similar sounds. Similarly, differential adaptation can be demonstrated when using two word-like stimuli that have been derived from human speech but adapted to the rat auditory system. Thus, differential adaptation to common and rare sounds is present also with sounds whose complexity mirrors that of natural environments.
Modular organization of the spinal motor system is thought to reduce the cognitive complexity of simultaneously controlling the large number of muscles and joints in the human body. Although modular organization has been confirmed in the hindlimb control system of several animal species, it has yet to be established in the forelimb motor system or in primates. Expanding upon experiments originally performed in the frog lumbar spinal cord, we examined whether costimulation of two sites in the macaque monkey cervical spinal cord results in motor activity that is a simple linear sum of the responses evoked by stimulating each site individually. Similar to previous observations in the frog and rodent hindlimb, our analysis revealed that in most cases (77% of all pairs) the directions of the force fields elicited by costimulation were highly similar to those predicted by the simple linear sum of those elicited by stimulating each site individually. A comparable simple summation of electromyography (EMG) output, especially in the proximal muscles, suggested that this linear summation of force field direction was produced by a spinal neural mechanism whereby the forelimb motor output recruited by costimulation was also summed linearly. We further found that the force field magnitudes exhibited supralinear (amplified) summation, which was also observed in the EMG output of distal forelimb muscles, implying a novel feature of primate forelimb control. Overall, our observations support the idea that complex movements in the primate forelimb control system are made possible by flexibly combined spinal motor modules.
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.
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...
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