Association learning-dependent increases in acetylcholine release in the rat auditory cortex during auditory classical conditioning

Butt, Allen E.; Chavez, Candice M.; Flesher, M. Melissa; Kinney-Hurd, Brandee L.; Araujo, Gabriel C.; Miasnikov, Alexandre A.; Weinberger, Norman M.

doi:10.1016/j.nlm.2009.05.006

Cited by 35 publications

(27 citation statements)

References 52 publications

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“…This factor provides unique opportunities for experimental control and determination of the neural mechanisms of memory and underscores the close linkage that can be found between the cholinergic system and the formation of associative memory. NB stimulation serves as a proxy for the release of acetylcholine in the auditory cortex, and such release has been verified by direct measurement during auditory associative learning (Butt, Chavez, Flesher, Kinney-Hurd, Araujo, Miasnikov, & Weinberger, 2009). Future studies that combine implantation of memory with the measurement of acetylcholine release are needed to more closely link the presumptive cholinergic cause with the formation of specific behavioral memory.…”

Section: Discussionmentioning

confidence: 91%

Consolidation and long-term retention of an implanted behavioral memory

Miasnikov¹,

Chen²,

Weinberger³

2011

Neurobiology of Learning and Memory

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Hypothesized circuitry enabling information storage can be tested by attempting to implant memory directly in the brain in the absence of normal experience. Previously, we found that tone paired with activation of the cholinergic nucleus basalis (NB) does induce behavioral memory that shares cardinal features with natural memory; it is associative, highly specific, rapidly formed, consolidates and shows intermediate retention. Here we determine if implanted memory also exhibits long-term consolidation and retention. Adult male rats were first tested for behavioral responses (disruption of ongoing respiration) to tones (1-15 kHz), yielding pre-training behavioral frequency generalization gradients. They next received three days of training with a conditioned stimulus (CS) tone (8.0 kHz, 70 dB, 2 s) either paired (n = 7) or unpaired (n = 6) with moderate electrical stimulation of the nucleus basalis (~65 μA, 100 Hz, 0.2 s, co-terminating with CS offset). Testing for long-term retention was performed by obtaining post-training behavioral frequency generalization gradients 24 h and 2 weeks after training. At 24 h post-training, the Paired group exhibited specific associative behavioral memory, manifested by larger responses to the CS frequency band than the Unpaired group. This memory was retained 2 weeks post-training. Moreover, two weeks later, the specificity and magnitude of memory had become greater, indicating that the implanted memory had undergone consolidation. Overall, the results demonstrate the validity of NB-implanted memory for understanding natural memory and that activation of the cholinergic nucleus basalis is sufficient to form natural associative memory.

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Section: Discussionmentioning

confidence: 91%

Consolidation and long-term retention of an implanted behavioral memory

Miasnikov¹,

Chen²,

Weinberger³

2011

Neurobiology of Learning and Memory

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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%

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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“…Area A1 is strongly innervated by cholinergic afferents, notably from the nucleus basalis (NB), which can induce strong local plasticity via muscarinic receptors (Ji et al 2001;Miasnikov et al 2001;Butt et al 2009;Froemke et al 2013). Electrically stimulating the NB during tone presentation alters the tuning of individual neurons (Froemke et al 2013) and remaps cortex to selectively expand the region representing the corresponding tone (Dimyan and Weinberger 1999) or other acoustic features like frequency sweeps and pulse sequences (Kilgard and Merzenich 1998a,b;Weinberger 1998;Kilgard et al 2001).…”

Section: Associative Plasticity In the Auditory Systemmentioning

confidence: 99%

Associative learning and sensory neuroplasticity: how does it happen and what is it good for?

McGann

2015

Learn. Mem.

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Historically, the body's sensory systems have been presumed to provide the brain with raw information about the external environment, which the brain must interpret to select a behavioral response. Consequently, studies of the neurobiology of learning and memory have focused on circuitry that interfaces between sensory inputs and behavioral outputs, such as the amygdala and cerebellum. However, evidence is accumulating that some forms of learning can in fact drive stimulus-specific changes very early in sensory systems, including not only primary sensory cortices but also precortical structures and even the peripheral sensory organs themselves. This review synthesizes evidence across sensory modalities to report emerging themes, including the systems' flexibility to emphasize different aspects of a sensory stimulus depending on its predictive features and ability of different forms of learning to produce similar plasticity in sensory structures. Potential functions of this learning-induced neuroplasticity are discussed in relation to the challenges faced by sensory systems in changing environments, and evidence for absolute changes in sensory ability is considered. We also emphasize that this plasticity may serve important nonsensory functions, including balancing metabolic load, regulating attentional focus, and facilitating downstream neuroplasticity.

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Association learning-dependent increases in acetylcholine release in the rat auditory cortex during auditory classical conditioning

Cited by 35 publications

References 52 publications

Consolidation and long-term retention of an implanted behavioral memory

Consolidation and long-term retention of an implanted behavioral memory

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

Associative learning and sensory neuroplasticity: how does it happen and what is it good for?

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