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  • Review Article
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Specific long-term memory traces in primary auditory cortex

Nature Reviews Neuroscience volume 5, pages 279–290 (2004)Cite this article

Key Points

  • Although the primary sensory cortices have traditionally been viewed as 'stimulus analysers', there is increasing evidence that they can undergo learning-associated plasticity. In the auditory cortex, pairing a tone with a weak shock can alter the subsequent response of the primary auditory cortex (A1) to the frequency of the tone. More recent studies have provided evidence for specificity of information storage, by combining the techniques of sensory physiology with learning and memory studies. Together, the findings indicate that A1 can store specific memory traces.

  • Changes that have been measured in A1 after learning include metabolic changes, shifts in receptive field tuning towards the conditioned stimulus frequency that occur rapidly and can last for weeks, and specific modifications of tonotopic maps to give a larger representation to the conditioned frequency. Imaging studies in humans have also shown specific, associative plasticity in A1. Together, the findings indicate that A1 can store specific memory traces.

  • Two main models have been proposed to account for such plasticity. Although they differ regarding the loci of plasticity, they agree on the importance of the nucleus basalis (NB) cholinergic system for long-term plasticity in A1. The NB is the main source of cortical acetylcholine (ACh), and cholinergic treatment of A1 causes lasting plasticity. Neurons in the NB respond to tone–shock conditioning and stimulation of the NB can substitute for a standard reinforcer in inducing plasticity in A1 and behavioural changes

  • The emerging picture of the function of A1 includes the analysis and storage of the behavioural significance of stimulus features such as frequency. Other cognitive functions for A1 are also being uncovered, including perceptual learning, rapid 'on-line' adjustments to maximize attentive captures of stimulus elements, learning of complex tasks, processing of abstract features and encoding planned behavioural acts. It will be necessary to integrate these functions and to develop a broader functional conceptualization of A1 and of the other primary sensory cortices.

Abstract

Learning and memory involve the storage of specific sensory experiences. However, until recently the idea that the primary sensory cortices could store specific memory traces had received little attention. Converging evidence obtained using techniques from sensory physiology and the neurobiology of learning and memory supports the idea that the primary auditory cortex acquires and retains specific memory traces about the behavioural significance of selected sounds. The cholinergic system of the nucleus basalis, when properly engaged, is sufficient to induce both specific memory traces and specific behavioural memory. A contemporary view of the primary auditory cortex should incorporate its mnemonic and other cognitive functions.

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Figure 1: The effects of learning on the frequency tuning of neurons in A1.
Figure 2: Development and retention of specific receptive field (RF) plasticity.
Figure 3: Specific tuning plasticity induced during appetitive conditioning revealed both in suprathreshold receptive field (RF) and threshold map measures.
Figure 4: Instrumental appetitive training with a normal reinforcer (bar press rewarded by water only in the presence of a 6-kHz tone) produces a specific increased representation that reflects the level of stimulus importance.
Figure 5: Two models of CS-specific tuning plasticity in the primary auditory cortex and fear conditioning.
Figure 6: CS-specific tuning plasticity induced by pairing a tone with stimulation of the nucleus basalis (NB), the major supplier of cortical acetylcholine.
Figure 7: Induction of specific behavioural memory by pairing a tone with stimulation of the nucleus basalis (NB).

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Acknowledgements

We gratefully acknowledge support by research grants from the National Institute of Deafness and Other Communication Disorders and from the National Institute of Mental Health.

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  1. Center for the Neurobiology of Learning and Memory and Department of Neurobiology and Behavior, University of California Irvine, Irvine, 92797-3800, California, USA

    Norman M. Weinberger

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Glossary

RECEPTIVE FIELD

That limited domain of the sensory environment to which a given sensory neuron is responsive, for example, a limited frequency band in audition or a limited area of space in vision.

TONOTOPIC MAP

An area in the auditory system in which neighbouring cells are most sensitive to acoustic frequencies that are adjacent to their own preferred threshold frequencies.

BRADYCARDIA

Slowing of heart rate. It is often a conditioned response to a stimulus that has been paired with a negative reinforcer.

SENSITIZATION

An increased response to a neutral stimulus caused by an increase in general arousal or behavioural excitability, often produced by presentation of a noxious stimulus.

BEST FREQUENCY

Within the receptive field for frequency of an auditory system neuron, the frequency that elicits the greatest cellular response.

CONSOLIDATION

A growth in the strength of memory across time after an experience, often inferred from increasing resistance to memory disruption with increasing time or directly measured as increasing strength of neural response over time.

NUCLEUS BASALIS

A group of neurons deep within the cerebral hemispheres that release acetylcholine (ACh) widely to the cerebral cortex.

CHARACTERISTIC FREQUENCY

The acoustic frequency to which an auditory neuron is tuned at its threshold of response.

FREQUENCY TUNING SHIFT

A change in the frequency tuning of an auditory neuron from its original best frequency to another frequency, often the result of increased behavioural importance of another frequency.

REINFORCER

A stimulus that is paired with and immediately follows presentation of a biologically neutral stimulus, such as a tone. Reinforcers are usually biologically important, such as food or shock.

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Weinberger, N. Specific long-term memory traces in primary auditory cortex. Nat Rev Neurosci 5, 279–290 (2004). https://doi.org/10.1038/nrn1366

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