Cholinergic Modulation of Experience-Dependent Plasticity in Human Auditory Cortex

Thiel, Christiane M.; Friston, Karl J.; Dolan, Raymond J.

doi:10.1016/s0896-6273(02)00801-2

Cited by 132 publications

(111 citation statements)

References 38 publications

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“…Complementing these findings, previous neuroimaging work in humans also revealed the rapid formation of learning-related changes in auditory cortex activity (Kluge et al, 2011;Morris, Friston, & Dolan, 1998;Thiel, Bentley, & Dolan, 2002;Thiel, Friston, & Dolan, 2002;van Wassenhove & Nagarajan, 2007). In line with animal data that show increased representations of the behaviorally relevant sound in auditory cortex, functional magnetic resonance imaging (fMRI) data in humans show increased BOLD responses to sounds, which have been paired with an electric shock to the foot in a classical conditioning experiment (Thiel, Bentley, et al, 2002;Thiel, Friston, et al, 2002).…”

Section: Learning-related Plasticity In Auditory Cortex: Animal and Hsupporting

confidence: 68%

“…Nowadays, neuroscientific methods, which range from single cell recordings of receptive fields in animals to the assessment of hemodynamic changes by means of functional imaging in humans, allow to investigate the neurobiological basis of such plasticity. In auditory cortex learningrelated changes have been demonstrated in a variety of associative learning paradigms in animals and men (for reviews see Schreiner & Polley, 2014;Thiel, 2007;Weinberger, 2007). In this paper we provide an overview of how the neurotransmitter dopamine modulates such learning-related plasticity, and how animal and human research can complement each other in providing an experimental approach that has relevance to studying mechanisms of recovery and treatment effects in patients with injuries.…”

Section: Introductionmentioning

confidence: 99%

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How dopamine shapes representations in auditory cortex

Puschmann

Weis

Thiel

2014

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Abstract. The neural representation of sound in the auditory cortex is not invariably predetermined by its acoustical properties, but it is constantly reshaped while the listener acquires new experiences. Such plastic changes are a prerequisite for lifelong learning and allow some degree of rehabilitation after brain injuries. Several neurotransmitter systems modulate these plastic changes. In this paper, we focus on how the neurotransmitter dopamine modulates learning-related plasticity in auditory cortex, and how animal and human research can complement each other in providing an experimental approach that has relevance for studying mechanisms of recovery of function.

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Section: Learning-related Plasticity In Auditory Cortex: Animal and Hsupporting

confidence: 68%

Section: Introductionmentioning

confidence: 99%

How dopamine shapes representations in auditory cortex

Puschmann

Weis

Thiel

2014

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“…Finally, influences from the amygdala to auditory cortex are known to be cholinergically mediated (via nucleus basalis; e.g., ref. 43), raising the intriguing possibility of applying pharmacological manipulations (10,(51)(52)(53) to our human MEG paradigm in future work.…”

Section: Discussionmentioning

confidence: 99%

“…Most research on auditory plasticity involved rodents, cats, or nonhuman primates, but some related evidence comes from human neuroimaging studies, with PET (8,9) or functional (f) MRI (10). Here, we used magnetoencephalography (MEG) (11,12) to address human auditory plasticity in an aversive classicalconditioning paradigm (1)(2)(3), focusing on the well-known, successive, auditory-evoked field components P1m, N1m, and P2m (13,14).…”

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confidence: 99%

Plasticity of human auditory-evoked fields induced by shock conditioning and contingency reversal

Kluge

Bauer

Leff

et al. 2011

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

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We used magnetoencephalography (MEG) to assess plasticity of human auditory cortex induced by classical conditioning and contingency reversal. Participants listened to random sequences of high or low tones. A first baseline phase presented these without further associations. In phase 2, one of the frequencies (CS + ) was paired with shock on half its occurrences, whereas the other frequency (CS − ) was not. In phase 3, the contingency assigning CS + and CS − was reversed. Conditioned pupil dilation was observed in phase 2 but extinguished in phase 3. MEG revealed that, during phase-2 initial conditioning, the P1m, N1m, and P2m auditory components, measured from sensors over auditory temporal cortex, came to distinguish between CS + and CS − . After contingency reversal in phase 3, the later P2m component rapidly reversed its selectivity (unlike the pupil response) but the earlier P1m did not, whereas N1m showed some new learning but not reversal. These results confirm plasticity of human auditory responses due to classical conditioning, but go further in revealing distinct constraints on different levels of the auditory hierarchy. The later P2m component can reverse affiliation immediately in accord with an updated expectancy after contingency reversal, whereas the earlier auditory components cannot. These findings indicate distinct cognitive and emotional influences on auditory processing.

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“…103). Stimulation of the NB or treatment with ACh promotes tone-shock pairing-induced tuning shifts in A1, whereas cholinergic antagonists or lesions of the NB have the opposite effect in animals [104][105][106] and humans 107 . Finally, NB neurons that project to A1 selectively increase transcription of the gene for choline acetyltransferase, which synthesizes ACh, during tone-shock conditioning, indicating that acoustic learning engages specific cholinergic subcellular mechanisms 108 .…”

Section: The Nb Cholinergic Systemmentioning

confidence: 99%

Specific long-term memory traces in primary auditory cortex

2004

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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.Identifying the neural substrates of learning and memory is a core problem in neuroscience. As memories involve the representation of past sensory events, they may be stored, in part, within sensory systems. Sensory systems have traditionally been viewed as 'stimulus analysers', with learning and memory assigned to 'higher' cortical regions. Nonetheless, neurophysiological studies have produced evidence for learning-induced plasticity in sensory cortices, and in particular the auditory cortex. Galambos and colleagues first implicated the primary auditory cortex (A1) in learning in 1956, observing that pairing an auditory conditioned stimulus (CS) with a weak shock (a mildly aversive unconditioned stimulus (US)) produced a significant increase in the amplitude of CS-elicited evoked field potentials in A1 of the cat 1 . Subsequently, these findings were extended to other tasks (such as discrimination), types of learning (including instrumental conditioning), motivations (for example, food) and types of recording (such as single and multiple unit discharges) 2 .Although such results established associative plasticity in A1, neither they nor similar findings in other sensory cortices addressed the key issue of specificity of information storage. As memories have specific content, how could changes in the magnitude of sensory cortical responses adequately reflect the encoding of specific aspects of experiences? A solution was provided by the field of sensory neurophysiology, which focuses on stimulus specificity. Sensory physiology experiments use a wide range of stimulus values to NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author Manuscript determine how specific sensory stimuli are processed and coded. In fact, the basic paradigms of sensory physiology and learning are complementary (Box 1).This article presents an overview of research that combines experimental designs from sensory physiology with those of learning and memory to search for specific memory traces in A1. A sign of a specific memory trace would be learning-induced physiological plasticity that has the key characteristics of behavioural memory and sufficient specificity to encode a canonical attribute of experience, such as a physical feature and its behavioural importance. Previous reviews have covered ot...

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Cholinergic Modulation of Experience-Dependent Plasticity in Human Auditory Cortex

Cited by 132 publications

References 38 publications

How dopamine shapes representations in auditory cortex

How dopamine shapes representations in auditory cortex

Plasticity of human auditory-evoked fields induced by shock conditioning and contingency reversal

Specific long-term memory traces in primary auditory cortex

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