Trial sequence of changed unit activity in auditory system of alert rat during conditioned response acquisition and extinction

Disterhoft, John F.; Stuart, Duncan K.

doi:10.1152/jn.1976.39.2.266

Cited by 87 publications

(38 citation statements)

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“…This hypothesis is consistent with the conditioning-induced plasticity of single auditory cortical neuron frequency response profiles elegantly documented by Edeline et al (1993) and Weinberger and Bakin (1998). Moreover, the results are consistent with earlier findings that the very first conditioning-related changes in neuronal firing occurred in the auditory cortex and were followed later by changes in the MG nucleus (Disterhoft and Stuart, 1976). Of course, the possibility exists that in addition to CS-US convergence, amygdalar modulation is also necessary for the establishment of MG nuclear plasticity during conditioning with just a single CS.…”

Section: Discussionsupporting

confidence: 92%

Amygdalar Efferents Initiate Auditory Thalamic Discriminative Training-Induced Neuronal Activity

Poremba

Gabriel

2001

J. Neurosci.

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It is well known that neurons of the medial geniculate (MG) nucleus of the thalamus send axonal projections to the amygdala. It has been proposed that these projections supply information that supports amygdalar associative processes underlying acquisition of acoustically cued conditioning and learning. Here we demonstrate the reverse direction of influence. Temporary inactivation of the amygdala using the GABA A receptor agonist muscimol just before the onset of discriminative avoidance conditioning permanently blocked the development of training-induced discriminative neuronal activity in the MG nucleus of rabbits. No discriminative activity developed when the amygdala was inactivated or during later training to criterion without muscimol. Thus, amygdalar processing at the outset of training is necessary for the development of training-induced discriminative activity of neurons in the MG nucleus.Key words: muscimol; GABA A agonist; temporary lesion; rabbits; associative conditioning; retention; multiunit neuronal activity It is well established that neurons in the amygdala and the medial geniculate (MG) nucleus, the auditory region of the sensory thalamus, are importantly involved in mediating acoustically cued Pavlovian and instrumental aversive conditioning Jarrell et al., 1986;LeDoux et al., 1986;McEchron et al., 1995;Maren and Fanselow, 1996;Davis, 1997; Poremba and Gabriel, 1997a,b;Armony et al., 1998;Ferry et al., 1999). Yet controversy remains as to the separate and distinct contributions of these nuclei, and little is known about how their neurons interact in mediating learning and performance.These issues could have been neatly resolved years ago had it been possible to confirm the hypothesis that neurons of the MG nucleus act simply to relay acoustic data to the amygdala via the direct axonal pathway documented by LeDoux et al. (1985). On this simple view, the function of MG nuclear neurons is sensory coding and transmission of acoustic signals. Interaction within the amygdala of the acoustic information with information concerning reinforcing stimuli would promote the development of plasticity at amygdalar synapses, which would thenceforth allow amygdalar neurons to respond uniquely to associatively significant acoustic cues, thus inducing the output of learned emotional responses and behaviors in other parts of the learning-relevant circuitry.A finding not easily incorporated into the foregoing model is the occurrence of training-induced associative neuronal activity, not simply sensory transmission, in the MG nucleus itself. For example, conditioning-induced, brief-latency discriminative neuronal activity develops in the medial region of the MG nucleus, and this activity exhibits reversal, during acquisition and reversal learning of a discriminative avoidance response (for review, see Gabriel et al., 1982). In the discriminative avoidance task, rabbits learn to avoid a foot shock by locomoting in response to a tone, the positive conditional stimulus (CSϩ), and they ignore a different tone, the CS...

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Section: Discussionsupporting

confidence: 92%

Amygdalar Efferents Initiate Auditory Thalamic Discriminative Training-Induced Neuronal Activity

Poremba

Gabriel

2001

J. Neurosci.

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“…In the trained animals, on the other hand, the spontaneous and tone-evoked activity of eight of the 14 available cells changed in the same FIG. 6 direction, and changed in the opposite direction in two cases, and one class of activity did not change significantly in four cases. These frequencies indicate an increased tendency for spontaneous and tone-evoked activity alterations to covary in the trained animals.…”

Section: Fig 5 Augmented Spontaneous Activity A-unitmentioning

confidence: 82%

“…They are dependent in part on nonacoustic variables such as the sleep-waking cycle (2, 3, 14, 18-ZO), experience (4,6,9,13,16), and anesthesia (7,8,10). Such nonsensory variables may be considered to determine the state of the animal.…”

Section: Introductionmentioning

confidence: 99%

Modulation of auditory cortex unit activity during the performance of a conditioned response

Kitzes

Farley

Starr

1978

Experimental Neurology

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Single-unit activity in primary auditory cortex was studied in unanesthetized, paralyzed cats during the performance of a classical conditioning task. The conditioned stimulus was a 0.5-s white noise (WN) burst paired with tail shock delivered 4.5 s later. Cats habituated to WN without shock served as controls. Overlayed on these tasks was a continuous background of l/s, behaviorally irrelevant, lOO-ms duration tone bursts set to the best frequency and optimal intensity for the particular unit being studied. Spontaneous activity and tone responses following WN were compared with the respective activity preceding WN. The spontaneous or evoked activity of 75% of the cells recorded in the trained animals changed significantly after WN, whereas the activity of 28% of the cells recorded in habituated animals changed. Augmentation and suppression of both spontaneous and evoked activity were found. These results have implications for the encoding of acoustic stimuli in terms of the modulation of lemniscal sensory system activity.

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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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Trial sequence of changed unit activity in auditory system of alert rat during conditioned response acquisition and extinction

Cited by 87 publications

References 0 publications

Amygdalar Efferents Initiate Auditory Thalamic Discriminative Training-Induced Neuronal Activity

Amygdalar Efferents Initiate Auditory Thalamic Discriminative Training-Induced Neuronal Activity

Modulation of auditory cortex unit activity during the performance of a conditioned response

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

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