Multiunit changes in hippocampus and medial geniculate body in free-behaving rats during acquisition and retention of a conditioned response to a tone

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

doi:10.1016/s0163-1047(88)90780-7

Cited by 40 publications

(25 citation statements)

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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.

204

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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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Section: Learning and Memory 11mentioning

confidence: 99%

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

Weinberger¹

2007

Learn. Mem.

204

190

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“…Reprinted from Weinberger (1995), with permission from MIT Press © 1995. Gabriel et al (1975) Rabbit Yes Gabriel et al (1976 Rabbit Yes Disterhoft and Stuart (1976) Rat Yes Ryugo and Weinberger (1978) Cat Yes Birt et al (1979) Rat Yes Birt and Olds (1981) Rat Yes Weinberger (1982) Cat Yes Jarrell et al (1986) Rabbit Yes LeDoux (1986) Rat Yes Edeline et al (1988) Rat Yes Supple and Kapp (1989) Rabbit Yes Edeline et al (1990) Rat Yes Edeline (1990) Rat Yes Edeline and Weinberger (1992) Guinea pig Yes Hennevin et al (1992) Rat Yes Lennartz and Weinberger (1992) However, as Suga has made the claims that his data are unblemished, it is customary for the claimant to provide evidence to support his own claims. Suga also wants us to determine if tuning shifts develop to repeated acoustic stimulation and if there is habituation to other frequencies.…”

Section: Proposed Experimentsmentioning

confidence: 99%

Retuning the brain by learning, literature, and logic: Reply to Suga

Weinberger¹

2008

Learn. Mem.

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Suga's Letter to the Editor in this issue (Suga 2008) is in response to my Review published in Learning & Memory early last year (Weinberger 2007). He objects to my characterization and critique of the Gao-Suga model. He also argues that our model is wrong in positing a key role for the magnocellular medial geniculate/posterior intralaminar nucleus (MGm/PIN) of the auditory thalamus in learning-induced auditory cortical tuning shifts and behavior. However, Suga's letter does not actually defend the Gao-Suga model (Suga and Ma 2003) that I reviewed. Rather, he sets forth a new (previously unpublished) version, without so informing the reader. He then attempts to nullify my critique that his original model omitted the MGm/PIN by discussing his new model, which does incorporate these nuclei, albeit with dubious functions. This slight-of-hand and other sweeping claims preclude the possibility of an adequate response in this limited format because more space is needed to explain errors of fact and logic than to promulgate them. Thus, we cannot include an adequate review of Suga's revised model. Neither can an explication, defense, or summary of our model and its tested predictions be presented. Readers should consult the target article for such information about our model and for a broad review of auditory associative representational plasticity (Weinberger 2007).Reply to Suga's responses to Weinberger's comments on the Gao-Suga modelIn this section, I discuss each of the six points raised by Suga, but in an order different than he used. I indicate the serial number of his points in brackets, to facilitate cross-referencing between our two Letters. The magnocellular medial geniculate nucleus [4]Much of my critique of Suga's model involves the fact that it completely ignores the MGm/PIN. This component of the thalamic auditory system receives convergent auditory and somatosensory (shock) information and projects to all regions of the auditory cortex and to the lateral amygdala. Suga's response is to the effect that he didn't ignore the MGm (see more below). Figure 1A presents Suga's original model. Inspection shows that the MGm/PIN and its important connections to the auditory cortex and amygdala are absent. Thus, Suga's original model does ignore the MGm.We can now consider Suga's revised model insofar as it includes the MGm/PIN (MGBm in his terminology). He argues that it is not involved in associative learning, particularly in fear conditioning. " Suga (2008) hypothesizes that the MGBm is involved in the non-specific plasticity (general augmentation) of cortical neurons elicited by unpaired CS and US (Fig. 1, dashed arrows) [ Fig. 1 Although he ignores the literature demonstrating associative plasticity in the MGm/PIN, Suga claims (earlier in his letter) that many laboratories have found tuning shifts ". . . without CS-US association in the MGBm and PIN." Suga cites 21 studies in support of his claim. One would then expect that at least some of these studies would have recorded in the MGm/PIN during the formation...

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“…Neurons of the MGv respond only to acoustic stimulation and are narrowly tuned to acoustic frequency [reviewed in Aitkin, 1990]. Of particular relevance, MGv cells are unchanged by learning [Gabriel et al, 1975;Ryugo and Weinberger, 1978;Birt and Olds, 1981;Edeline et al, 1988;Edeline and Weinberger, 1992]. Furthermore, MGv cells either do not develop RF plasticity or exhibit only transient plasticity of less than 1 h [Edeline .…”

Section: Components Of the Modelmentioning

confidence: 99%

“…In contrast to the MGv, the MGm is greatly affected by learning. Its neurons develop learning-induced increased responses to acoustic CS during classical conditioning trials, including differential neuronal plasticity during discrimination training to two acoustic stimuli [Gabriel et al, 1975;Ryugo and Weinberger, 1978;Birt and Olds, 1981;Weinberger, 1982;Edeline et al, 1988;Edeline and Weinberger, 1992]. Furthermore, they develop specific, long-lasting RF plasticity [Edeline and Weinberger, 1992].…”

Section: Components Of the Modelmentioning

confidence: 99%

Learning-Induced Physiological Memory in Adult Primary Auditory Cortex: Receptive Field Plasticity, Model, and Mechanisms

1998

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It is well established that the functional organization of adult sensory cortices, including the auditory cortex, can be modified by deafferentation, sensory deprivation, or selective sensory stimulation. This paper reviews evidence establishing that the adult primary auditory cortex develops physiological plasticity during learning. Determination of frequency receptive fields before and at various times following aversive classical conditioning and instrumental avoidance learning in the guinea pig reveals increased neuronal responses to the pure tone frequency used as a conditioned stimulus (CS). In contrast, responses to the pretraining best frequency and other non-CS frequencies are decreased. These opposite changes are often sufficient to shift cellular tuning toward or even to the frequency of the CS. Learning-induced receptive field (RF) plasticity (i) is associative (requires pairing tone and shock), (ii) highly specific to the CS frequency (e.g., limited to this frequency ± a small fraction of an octave), (iii) discriminative (specific increased response to a reinforced CS+ frequency but decreased response to a nonreinforced CS– frequency), (iv) develops extremely rapidly (within 5 trials, the fewest trials tested), and (v) is retained indefinitely (tested to 8 weeks). Moreover, RF plasticity is robust and not due to arousal, but can be expressed in the deeply anesthetized subject. Because learning- induced RF plasticity has the major characteristics of associative memory, it is therefore referred to as ‘physiological memory.’ We developed a model of RF plasticity based on convergence in the auditory cortex of nucleus basalis cholinergic effects acting at muscarinic receptors, with lemniscal and nonlemniscal frequency information from the ventral and magnocellular divisions of the medial geniculate nucleus, respectively. In the model, the specificity of RF plasticity is dependent on Hebbian rules of covariance. This aspect was confirmed in vivo using microstimulation techniques. Further, the model predicts that pairing a tone with activation of the nucleus basalis is sufficient to induce RF plasticity similar to that obtained in behavioral learning. This prediction has been confirmed. Additional tests of the model are described. RF plasticity is thought to translate the acquired significance of sound into an increased frequency representation of behaviorally important stimuli.

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Multiunit changes in hippocampus and medial geniculate body in free-behaving rats during acquisition and retention of a conditioned response to a tone

Cited by 40 publications

References 39 publications

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

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

Retuning the brain by learning, literature, and logic: Reply to Suga

Learning-Induced Physiological Memory in Adult Primary Auditory Cortex: Receptive Field Plasticity, Model, and Mechanisms

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