Receptive field plasticity in the auditory cortex during frequency discrimination training: Selective retuning independent of task difficulty.

Edeline, Jean‐Marc; Weinberger, Norman M.

doi:10.1037/0735-7044.107.1.82

Cited by 184 publications

(142 citation statements)

References 35 publications

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“…The lack of plasticity in the STD group might seem inconsistent with prior findings of specific A1 plasticity in both classical (Bakin & Weinberger, 1990;Edeline & Weinberger, 1993;Gonzalez-Lima & Scheich, 1986b;Ohl & Scheich, 1996) and instrumental avoidance (Bakin et al, 1996) fear conditioning. Fear conditioning studies have concentrated on changes in receptive field tuning and have not studied possible modifications in threshold or bandwidth.…”

Section: Auditory Learning Without Auditory Cortical Plasticitycontrasting

confidence: 91%

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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Section: Auditory Learning Without Auditory Cortical Plasticitycontrasting

confidence: 91%

Learning strategy determines auditory cortical plasticity

Berlau

Weinberger

2008

Neurobiology of Learning and Memory

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“…Thus, taken together, the ECM influences short-and longterm plasticity of synapses and thereby potentially regulates signal processing within a neuronal network during learning. Indeed, auditory associative learning has been correlated with structural changes of topographic connections within primary ACx (19,(29)(30)(31), changes in interneuron activity (32,33), and Ca 2+ -dependent synaptic processing (34). However, further work will have to investigate the exact cellular and network effects of ECM removal in sensory cortex during learning processes in vivo.…”

Section: Potential Cellular Mechanisms Of Ecm-derived Modulation Ofmentioning

confidence: 99%

Enhanced cognitive flexibility in reversal learning induced by removal of the extracellular matrix in auditory cortex

Happel

Niekisch²,

Rivera³

et al. 2014

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

144

118

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During brain maturation, the occurrence of the extracellular matrix (ECM) terminates juvenile plasticity by mediating structural stability. Interestingly, enzymatic removal of the ECM restores juvenile forms of plasticity, as for instance demonstrated by topographical reconnectivity in sensory pathways. However, to which degree the mature ECM is a compromise between stability and flexibility in the adult brain impacting synaptic plasticity as a fundamental basis for learning, lifelong memory formation, and higher cognitive functions is largely unknown. In this study, we removed the ECM in the auditory cortex of adult Mongolian gerbils during specific phases of cortex-dependent auditory relearning, which was induced by the contingency reversal of a frequency-modulated tone discrimination, a task requiring high behavioral flexibility. We found that ECM removal promoted a significant increase in relearning performance, without erasing already establishedthat is, learned-capacities when continuing discrimination training. The cognitive flexibility required for reversal learning of previously acquired behavioral habits, commonly understood to mainly rely on frontostriatal circuits, was enhanced by promoting synaptic plasticity via ECM removal within the sensory cortex. Our findings further suggest experimental modulation of the cortical ECM as a tool to open short-term windows of enhanced activitydependent reorganization allowing for guided neuroplasticity.chondroitin sulfate proteoglycan | hyaluronidase | perineuronal net | intracortical microinjection | strategy change S tructural remodeling and stabilization of synaptic networks are key mechanisms underlying learning in the adult brain. During early life, high structural and functional plasticity is required for the experience-shaped development of basic neuronal circuits (1). With brain maturation, juvenile plasticity of so-called critical or sensitive periods is decreased and is accompanied by the appearance of the brain's extracellular matrix (ECM) and its specialized compact form named "perineuronal net" (PNN) enwrappping cell bodies and synaptic contacts (2, 3). Enzymatic degradation of the ECM in adult animals has been demonstrated to restore such forms of developmental (juvenile) plasticity with respect to topographical map plasticity in the visual cortex (4), fearresponse-mediating circuits in the amygdala (5), spinal cord injuries (6, 7), and song learning circuits of zebra finches (8). In addition, enzymatic ECM removal altered several forms of synaptic plasticity in vitro and in vivo (9-12). However, even though structural stability of networks acquired during developmental phases is essential for neuronal efficiency, mechanisms allowing synaptic remodeling are key events during learning and memory formation throughout life (13). We recently demonstrated that endogenous proteases moderately digesting specific components of the ECM are regulated in an activity-dependent manner (2, 14) and ECM removal modulates synaptic short-term plasticity by synaptic e...

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“…Though a previous study (Sakurai, 1990b) has shown that neurons in AC are involved in sensory discrimination and retention for WM, the present study indicates that AC neurons are involved in those processes not only for WM but also for RM. These functions of AC could be predicted from learning-induced changes of activity of AC neurons (Edeline et al, 1990) and learning-induced plasticity of receptive fields in AC (Weinberger et al, 1990;Edeline and Weinberger, 1993). Especially with regard to retention by AC neurons, the posttone facilitation of activity of AC units during the sequential presentation of tones (McKenna et al, 1989) might be related to a mechanism underlying the retention.…”

Section: Unique Functions Of the Auditory Cortexmentioning

confidence: 99%

“…These responses are surely taskperformance dependent, because the neurons showed no specific responses to the tones at times when there was no memory task. A recent study showing receptive field plasticity in the AC during frequency discrimination training (Edeline and Weinberger, 1993) also indicates the flexibility of AC neurons for learned task performance.…”

Section: Unique Functions Of the Auditory Cortexmentioning

confidence: 99%

Involvement of auditory cortical and hippocampal neurons in auditory working memory and reference memory in the rat

Sakurai

1994

J. Neurosci.

122

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The goal of the present study was to see whether one neuron is involved exclusively in one type of memory or in different types of memory. Single-unit activity was recorded from rat hippocampal CAl, CA3, dentate gyrus, and auditory cortex (AC) during performances of auditory working memory (WM) and reference memory (RM) tasks. Both the memory tasks employed identical apparatus and stimuli and differed only in the type of memory required for correct performance.Around 10% and 43% of the units from the four brain regions showed sensory correlates (differences in activity due to the type of sensory stimulus) only in the WM or RM task, respectively.Only the AC had units showing different kinds of sensory correlates between the WM and RM tasks. About 30% of the units from the four regions had sensoryretention correlates (sustained differential activity during the delay) only in the RM task, whereas the AC had units with sensory-retention correlates only in the WM task or in both the WM and RM tasks. Approximately 35% of the units from the hippocampal regions showed motor correlates (increments of activity immediately prior to responses) only in the WM task. Another 30% of the hippocampal units showed such correlates both in the WM and RM tasks. About 22% of the hippocampal CA1 and CA3 units showed comparisonmotor correlates (increases of activity prior to correct responses) only in the WM task.These results indicate that some neurons are involved solely in WM or RM, whereas other neurons are involved in both WM and RM. The results also suggest that more neurons are involved in sensory and retention processing for RM than for WM, and that the AC alone has flexible neurons involved in the processes for both types of memory. More hippocampal neurons are involved in the motor and comparison processes for WM than for RM.

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Receptive field plasticity in the auditory cortex during frequency discrimination training: Selective retuning independent of task difficulty.

Cited by 184 publications

References 35 publications

Learning strategy determines auditory cortical plasticity

Learning strategy determines auditory cortical plasticity

Enhanced cognitive flexibility in reversal learning induced by removal of the extracellular matrix in auditory cortex

Involvement of auditory cortical and hippocampal neurons in auditory working memory and reference memory in the rat

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