Discriminative long-term retention of rapidly induced multiunit changes in the hippocampus, medial geniculate and auditory cortex

Edeline, Jean‐Marc; Massioui, Nicole Neuenschwander-El; Dutrieux, Gérard

doi:10.1016/0166-4328(90)90101-j

Cited by 58 publications

(33 citation statements)

References 37 publications

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“…NIH-PA Author Manuscript NIH-PA Author Manuscript because MGm RFs are much more complex, multipeaked and broadly tuned than those of auditory cortical cells [55][56][57] . Therefore, long-term, specific plasticity in A1 is not merely a reflection of plasticity in the subcortical auditory system but probably reflects processes in the cortex.…”

Section: Nih-pa Author Manuscriptmentioning

confidence: 99%

“…The Suga model ignores the MGm, its intrinsic associative plasticity and its influences on both A1 and the lateral amygdala (LA), but the following findings directly implicate the MGm: acoustic and nociceptive information converge directly in the MGm 58,59 ; associative learning is accompanied by the development of plasticity in the MGm [60][61][62][63][64][65][66] , which is longlasting 63 and is evident as CS-specific RF plasticity after conditioning 56,67 ; the MGm holds an associative memory trace after CS offset during conditioning 68 ; analogues of learning show that stimulation of the MGm induces long-term potentiation in A1 (REF. 69) and tone paired with stimulation of the MGm induces heterosynaptic long-term potentiation in A1 (REF.…”

Section: Loci Of Plasticitymentioning

confidence: 99%

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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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Section: Nih-pa Author Manuscriptmentioning

confidence: 99%

Section: Loci Of Plasticitymentioning

confidence: 99%

Specific long-term memory traces in primary auditory cortex

2004

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“…It projects to Layer I and the apical dendrites of pyramidal cells in A1 and in all other auditory cortical fields (Winer and Morest 1983) and does so via giant axons that provide the fastest thalamo-cortical transmission (Huang and Winer 2000). In addition to findings listed above that implicate the MGm (and its related posterior intralaminar nucleus [PIN]) in associative learning, this structure is well known to develop associative plasticity during conditioning (Gabriel et al 1975(Gabriel et al , 1976Disterhoft and Stuart 1976;Birt et al 1979;Birt and Olds 1981;Weinberger 1982;Jarrell et al 1986b;LeDoux et al 1986b;Edeline et al 1988Edeline et al , 1990Edeline 1990;McEchron et al 1995McEchron et al , 1996Hennevin et al 1998). Moreover, its stimulation induces in the auditory cortex heterosynaptic (Weinberger et al 1995) long-term potentiation (LTP), which has been implicated in learning (see also Parsons et al 2006).…”

Section: Learning and Memory 11mentioning

confidence: 99%

Associative representational plasticity in the auditory cortex: A synthesis of two disciplines

Weinberger¹

2007

Learn. Mem.

203

190

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Historically, sensory systems have been largely ignored as potential loci of information storage in the neurobiology of learning and memory. They continued to be relegated to the role of "sensory analyzers" despite consistent findings of associatively induced enhancement of responses in primary sensory cortices to behaviorally important signal stimuli, such as conditioned stimuli (CS), during classical conditioning. This disregard may have been promoted by the fact that the brain was interrogated using only one or two stimuli, e.g., a CS + sometimes with a CS -, providing little insight into the specificity of neural plasticity. This review describes a novel approach that synthesizes the basic experimental designs of the experimental psychology of learning with that of sensory neurophysiology. By probing the brain with a large stimulus set before and after learning, this unified method has revealed that associative processes produce highly specific changes in the receptive fields of cells in the primary auditory cortex (A1). This associative representational plasticity (ARP) selectively facilitates responses to tonal CSs at the expense of other frequencies, producing tuning shifts toward and to the CS and expanded representation of CS frequencies in the tonotopic map of A1. ARPs have the major characteristics of associative memory: They are highly specific, discriminative, rapidly acquired, exhibit consolidation over hours and days, and can be retained indefinitely. Evidence to date suggests that ARPs encode the level of acquired behavioral importance of stimuli. The nucleus basalis cholinergic system is sufficient both for the induction of ARPs and the induction of specific auditory memory. Investigation of ARPs has attracted workers with diverse backgrounds, often resulting in behavioral approaches that yield data that are difficult to interpret. The advantages of studying associative representational plasticity are emphasized, as is the need for greater behavioral sophistication.

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“…The magnocellular medial geniculate body provides nonlemniscal input to upper layers of the auditory cortex. Its cells do develop increased responses to the CS during training, and their RFs are retuned to favor the CS frequency (Edeline & Weinberger 1992, Edeline et al 1990b, Lennartz & Weinberger 1992b). However, their RFs are much more complex and broadly tuned than those of auditory cortical cells, so it seems unlikely that the highly frequency-specific cortical RF plasticity is simply projected from this nucleus, although this cannot yet be discounted.…”

Section: Possible Mechanisms Of Rf Plasticity and Map Reorganization mentioning

confidence: 99%

Dynamic Regulation of Receptive Fields and Maps in the Adult Sensory Cortex

Weinberger¹

1995

Annual Review of Neuroscience

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Discriminative long-term retention of rapidly induced multiunit changes in the hippocampus, medial geniculate and auditory cortex

Cited by 58 publications

References 37 publications

Specific long-term memory traces in primary auditory cortex

Specific long-term memory traces in primary auditory cortex

Associative representational plasticity in the auditory cortex: A synthesis of two disciplines

Dynamic Regulation of Receptive Fields and Maps in the Adult Sensory Cortex

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