Working Memory-Specific Activity in Auditory Cortex: Potential Correlates of Sequential Processing and Maintenance

Brechmann, André; Gaschler‐Markefski, Birgit; Sohr, Mandy; Yoneda, Koichi; Kaulisch, Thomas; Scheich, Henning

doi:10.1093/cercor/bhl160

Cited by 51 publications

(51 citation statements)

References 67 publications

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“…For example, it is possible that those primary areas not only represent modalityspecific sensory information while a stimulus is presented, but also are able to maintain some of that information ''on line'' during the working memory period of a discrimination task, and perhaps even participate in the subsequent decision-making steps. For instance, there are several reports suggesting that primary sensory cortices are involved to some degree in working memory tasks (34)(35)(36). Furthermore, a recent study has shown that, in addition to representing acoustic features, responses in A1 and R auditory fields may serve to encode some cognitive task elements associated with auditory processing (29), which also seems consistent with the idea that auditory cortex becomes selective to other sensory modalities when these are associated with auditory processing during action selection (29).…”

Section: Discussionsupporting

confidence: 63%

Neural codes for perceptual discrimination of acoustic flutter in the primate auditory cortex

Lemus

Hernandez

Romo

2009

Proc. Natl. Acad. Sci. U.S.A.

106

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We recorded from single neurons of the primary auditory cortex (A1), while trained monkeys reported a decision based on the comparison of 2 acoustic flutter stimuli. Crucially, to form the decision, monkeys had to compare the second stimulus rate to the memory trace of the first stimulus rate. We found that the responses of A1 neurons encode stimulus rates both through their periodicity and through their firing rates during the stimulation periods, but not during the working memory and decision components of this task. Neurometric thresholds based on firing rate were very similar to the monkey's discrimination thresholds, whereas neurometric thresholds based on periodicity were lower than the experimental thresholds. Thus, an observer could solve this task with a precision similar to that of the monkey based only on the firing rates evoked by the stimuli. These results suggest that the A1 is exclusively associated with the sensory and not with the cognitive components of this task.decision making ͉ monkeys ͉ working memory ͉ psychophysics ͉ neurophysiology T he problem of how sensory experiences arise from activity in the brain has stimulated a large amount of research in neuroscience (1, 2). A major component of this problem involves understanding how the brain represents sensory features-that is, what attributes of the neural responses evoked by a stimulus are meaningful for sensation, perception, memory, and decisionmaking? To confront these issues unambiguously, experimental methods should conform to 2 essential conditions: first, the sensory stimulus must be under precise, quantitative control, and second, the subject's psychophysical responses should be well controlled and quantitatively measured. Most experimental paradigms meeting these standards have involved vision (1, 3) and somatosensation (2, 4). In comparison, the amount of research about audition using this approach is scant (5). Most of the studies in the auditory cortex and related areas have described the response properties of neurons to auditory scenes in anesthetized and awake animals, and how these are affected by different task conditions (5-21). But how the neural representations of acoustic stimuli are related to perception, memory and decision making is not known.We addressed this problem by recording the activity of single neurons in the primary auditory cortex (A1), while trained monkeys discriminated the difference in rate of 2 acoustic flutter stimuli (range of 4-40 Hz). The sensation of acoustic flutter is produced by slow repetition of an acoustic stimulus (11). The rate of the acoustic flutter is determined by the interval between the acoustic stimuli (pulse trains). In the acoustic flutter discrimination task, monkeys report whether the second stimulus rate (f2) is higher or lower than the first stimulus rate (f1). This cognitive operation requires that subjects compare information of f2 with a stored trace of f1 to form a decision, that is, whether f2 Ͼ f1 or f2 Ͻ f1, and to report their perceptual evaluation after a short, fix...

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Section: Discussionsupporting

confidence: 63%

Neural codes for perceptual discrimination of acoustic flutter in the primate auditory cortex

Lemus

Hernandez

Romo

2009

Proc. Natl. Acad. Sci. U.S.A.

106

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“…But because only right AC seems able to explicitly distinguish a rising from a falling continuous FM, it must be assumed that an interaction with other parts of cortex that serve the behavioral consequences of this task is selectively established with right AC. This idea of flexible task-dependent interactions in cortex is much supported by human fMRI results (44,45) and by anatomical evidence. Unlike subcortical auditory stations where processing steps can be explained by convergent and divergent ascending inputs, even primary AC receives Ͼ50% of its inputs from other cortical areas including many nonauditory fields (60).…”

Section: Discussionmentioning

confidence: 79%

“…In human functional (f)MRI experiments, we found that the categorization of direction of FM stimuli produced dominant blood-oxygen leveldependent (BOLD) activation of right AC, but categorization of their duration resulted in activation of left AC (44). Moreover, a matching-to-sample task with the same FM stimuli in serial comparisons generated dominant left AC activations (45). Similarly, in a ''streaming'' task, where the selective segmental comparison of stimuli is crucial, BOLD activation was lateralized to the left AC (46).…”

mentioning

confidence: 93%

“…In our animal model (42), we lesioned ACs of gerbils bilaterally or unilaterally and trained them before and after lesions on various discriminations of linearly FM tone sweeps that were either continuous or segmented. Based on our previous lateralization studies in gerbils (42) and humans (44)(45)(46) and considering the related data of other authors (6, 13, 49), we used artificial stimuli that varied along spectral and temporal dimensions (see Table 1). In gerbils, a hypertrophied middle-ear cavity results in increased low-frequency hearing, a feature that seems to be important in a desert environment where it is necessary to escape from predators, e.g., owls and snakes that produce frequencies in the range of 1-2 kHz.…”

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confidence: 99%

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Global versus local processing of frequency-modulated tones in gerbils: An animal model of lateralized auditory cortex functions

Wetzel

Ohl

Scheich

2008

Proc. Natl. Acad. Sci. U.S.A.

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Hemispheric asymmetries of speech and music processing might arise from more basic specializations of left and right auditory cortex (AC). It is not clear, however, whether such asymmetries are unique to humans, i.e., consequences of speech and music, or whether comparable lateralized AC functions exist in nonhuman animals, as evolutionary precursors. Here, we investigated the cortical lateralization of perception of linearly frequency-modulated (FM) tones in gerbils, a rodent species with human-like lowfrequency hearing. Using a footshock-reinforced shuttle-box avoidance go/no-go procedure in a total of 178 gerbils, we found that (i) the discrimination of direction of continuous FM (rising versus falling sweeps, 250-ms duration) was impaired by right but not left AC lesions; (ii) the discrimination of direction of segmented FM (50-ms segments, 50-ms silent gaps, total duration 250 ms) was impaired by bilateral but not unilateral AC lesions; (iii) the discrimination of gap durations (10 -30 ms) in segmented FM was impaired by left but not right AC lesions. AC lesions before and after training resulted in similar effects. Together, these experiments suggest that right and left AC, even in rodents, use different strategies in analyzing FM stimuli. Thus, the right AC, by using global cues, determines the direction of continuous and segmented FM but cannot discriminate gap durations. The left AC, by using local cues, discriminates gap durations and determines FM direction only when additional segmental information is available.asymmetry ͉ lateralization ͉ rodents

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“…Learning-related plasticity in A1 develops in a wide range of tasks, including habituation (Condon &Weinberger, 1991), classical reward (Kisley & Gerstein, 2001) and aversive (Bakin & Weinberger, 1990) conditioning, instrumental reward (Blake et al, 2002) and avoidance (Bakin, South, & Weinberger, 1996) learning, category learning (Ohl, Scheich, & Freeman, 2001), long-term training in perceptual discrimination learning (Recanzone, Schreiner, & Merzenich, 1993), working memory (Brechmann et al, 2007;Sakurai, 1994), reference memory (Sakurai, 1994) and motor planning (Villa, Tetko, Hyland, & Najem, 1999). A dominant finding has been that sounds which acquire behavioral significance receive "favored" processing, e.g., as indexed by specific increased magnitude of response and CSdirected tuning shifts.…”

Section: Introductionmentioning

confidence: 99%

Learning strategy determines auditory cortical plasticity

Berlau

Weinberger

2008

Neurobiology of Learning and Memory

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Learning modifies the primary auditory cortex (A1) to emphasize the processing and representation of behaviorally relevant sounds. However, the factors that determine cortical plasticity are poorly understood. While the type and amount of learning are assumed to be important, the actual strategies used to solve learning problems might be critical. To investigate this possibility, we trained two groups of adult male Sprague-Dawley rats to bar-press (BP) for water contingent on the presence of a 5.0 kHz tone using two different strategies: BP during tone presence or BP from tone-onset until receiving an error signal after tone cessation. Both groups achieved the same high levels of correct performance and both groups revealed equivalent learning of absolute frequency during training. Post-training terminal "mapping" of A1 showed no change in representational area of the tone signal frequency but revealed other substantial cuespecific plasticity that developed only in the tone-onset-to-error strategy group. Threshold was decreased ~10 dB and tuning bandwidth was narrowed by ~0.7 octaves. As sound onsets have greater perceptual weighting and cortical discharge efficacy than continual sound presence, the induction of specific learning-induced cortical plasticity may depend on the use of learning strategies that best exploit cortical proclivities. The present results also suggest a general principle for the induction and storage of plasticity in learning, viz., that the representation of specific acquired information may be selected by neurons according to a match between behaviorally selected stimulus features and circuit/network response properties.

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Working Memory-Specific Activity in Auditory Cortex: Potential Correlates of Sequential Processing and Maintenance

Cited by 51 publications

References 67 publications

Neural codes for perceptual discrimination of acoustic flutter in the primate auditory cortex

Neural codes for perceptual discrimination of acoustic flutter in the primate auditory cortex

Global versus local processing of frequency-modulated tones in gerbils: An animal model of lateralized auditory cortex functions

Learning strategy determines auditory cortical plasticity

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