Intrinsic neurons in the amygdaloid field projected to by the medial geniculate body mediate emotional responses conditioned to acoustic stimuli

Iwata, Jiro; LeDoux, Joseph E.; Meeley, Mary P.; Arnerić, Stephen P.; Reis, Donald J.

doi:10.1016/0006-8993(86)90020-x

Cited by 268 publications

(168 citation statements)

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“…69) and tone paired with stimulation of the MGm induces heterosynaptic long-term potentiation in A1 (REF. 70) and behavioural conditioning 71 ; lesions of the MGm interfere with auditory input to the amygdala during conditioning [72][73][74] ; the MGm develops synaptic plasticity during conditioning and does so with a shorter latency than does the amygdala 65 ; and fear conditioning produces increased presynaptic release of transmitter (glutamate) in MGm cells that project to the LA 75 . Selective lesions of the MGm should impair cortical RF plasticity, although this has not been tested.…”

Section: Nih-pa Author Manuscriptmentioning

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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Section: Nih-pa Author Manuscriptmentioning

confidence: 99%

Specific long-term memory traces in primary auditory cortex

2004

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Section: Abstract: Limbic Thalamus; Cingulate Cortex; Amygdala; Learmentioning

confidence: 99%

“…An involvement of the medial geniculate (MG) nucleus in aversively motivated learning is indicated by the observation of TIA in the medial division of the MG nucleus (MGm) (Olds et al., 1972;Gabriel et al, 1975;Gabriel et al, 1976;Ryugo and Weinberger, 1978;Birt and Olds, 1981;Weinberger, 1982;Edeline, 1990;Edeline and Weinberger, 1992;McEchron et al, 1995), and by impaired conditioning in animals with MG lesions (Iwata et al, 1986;Jarrell et al, 1986; LeDoux et al, 1986a,b;McCabe et al, 1993). Amygdalar and MG neurons are involved in aversively motivated instrumental conditioning processes, as well as in classical aversive conditioning.…”

Section: Abstract: Limbic Thalamus; Cingulate Cortex; Amygdala; Learmentioning

confidence: 99%

“…A central role of amygdalar neurons is indicated by findings that amygdala lesions impair the acquisition of conditioned immobility (LeDoux et al, 1988; Fanselow and K im, 1994;LeDoux, 1995), autonomic responding (Blanchard and Blanchard, 1972;Spevack et al, 1975;Kapp et al, 1979;Gentile et al, 1986;Iwata et al, 1986;Helmstetter, 1992) and fear-potentiated startle behavior (Davis, 1986(Davis, , 1992Hitchcock and Davis, 1987;Sananes and Davis, 1992). Also, amygdalar neurons exhibit associative, training-induced activity (TIA) during Pavlovian conditioning (Umemoto and Olds, 1975;Applegate et al, 1982;Pascoe and Kapp, 1985;Nishijo et al, 1988; Muramoto et al, 1993;McEchron et al, 1995;Quirk et al, 1995).An involvement of the medial geniculate (MG) nucleus in aversively motivated learning is indicated by the observation of TIA in the medial division of the MG nucleus (MGm) (Olds et al., 1972;Gabriel et al, 1975;Gabriel et al, 1976;Ryugo and Weinberger, 1978;Birt and Olds, 1981;Weinberger, 1982;Edeline, 1990;Edeline and Weinberger, 1992;McEchron et al, 1995), and by impaired conditioning in animals with MG lesions (Iwata et al, 1986;Jarrell et al, 1986; LeDoux et al, 1986a,b;McCabe et al, 1993). Amygdalar and MG neurons are involved in aversively motivated instrumental conditioning processes, as well as in classical aversive conditioning.…”

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Medial Geniculate Lesions Block Amygdalar and Cingulothalamic Learning-Related Neuronal Activity

Poremba

Gabriel

1997

J. Neurosci.

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This study assessed the role of the thalamic medial geniculate (MG) nucleus in discriminative avoidance learning, wherein rabbits acquire a locomotory response to a tone [conditioned stimulus (CS)ϩ] to avoid a foot shock, and they learn to ignore a different tone (CSϪ) not predictive of foot shock. Limbic (anterior and medial dorsal) thalamic, cingulate cortical, or amygdalar lesions severely impair acquisition, and neurons in these areas develop training-induced activity (TIA): more firing to the CSϩ than to the CSϪ. MG neurons exhibit TIA during learning and project to the amygdala. The MG neurons may supply afferents essential for amygdalar and cingulothalamic TIA and for avoidance learning. To test this hypothesis, bilateral electrolytic or excitotoxic ibotenic acid MG nuclear lesions were induced, and multiunit recording electrodes were chronically implanted into the anterior and posterior cingulate cortex, the anterior-ventral and medial-dorsal thalamic nuclei, and the basolateral nucleus of the amygdala before training. Learning was severely impaired and TIA was abolished in all areas in rabbits with lesions. Thus learning and TIA require the integrity of the MG nucleus. Only damage in the medial MG division was significantly correlated with the learning deficit. The lesions abolished the sensory response of amygdalar neurons, and they attenuated (but did not eliminate) the sensory response of cingulothalamic neurons, suggesting the existence of extra geniculate sources of auditory transmission to the cingulothalamic areas. Key words: limbic thalamus; cingulate cortex; amygdala; learning; instrumental conditioning; anterior ventral nucleus; medial dorsal nucleusThere is currently a great interest in the neural circuitry underlying aversively motivated learning (for review, see Davis, 1992;Gabriel, 1993;Lennartz and Weinberger, 1994;LeDoux, 1995;McGaugh et al., 1995;. A central role of amygdalar neurons is indicated by findings that amygdala lesions impair the acquisition of conditioned immobility (LeDoux et al., 1988; Fanselow and K im, 1994;LeDoux, 1995), autonomic responding (Blanchard and Blanchard, 1972;Spevack et al., 1975;Kapp et al., 1979;Gentile et al., 1986;Iwata et al., 1986;Helmstetter, 1992) and fear-potentiated startle behavior (Davis, 1986(Davis, , 1992Hitchcock and Davis, 1987;Sananes and Davis, 1992). Also, amygdalar neurons exhibit associative, training-induced activity (TIA) during Pavlovian conditioning (Umemoto and Olds, 1975;Applegate et al., 1982;Pascoe and Kapp, 1985;Nishijo et al., 1988; Muramoto et al., 1993;McEchron et al., 1995;Quirk et al., 1995).An involvement of the medial geniculate (MG) nucleus in aversively motivated learning is indicated by the observation of TIA in the medial division of the MG nucleus (MGm) (Olds et al., 1972;Gabriel et al., 1975;Gabriel et al., 1976;Ryugo and Weinberger, 1978;Birt and Olds, 1981;Weinberger, 1982;Edeline, 1990;Edeline and Weinberger, 1992;McEchron et al., 1995), and by impaired conditioning in animals with MG lesions (Iwata et al., 198...

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“…The central circuitry mediating the classical conditioning of fear to an acoustic stimulus in rats involves transmission through primary auditory structures of the brain stem to the auditory receptive region of the thalamus and, from there, directly to the amygdala (LeDoux et al, 1984LeDoux, 1986LeDoux, , 1987Iwata et al, 1986a). The critical amygdaloid regions are located in the dorsal part of this structure, and include the lateral and central nuclei and the amygdalostriatal transition zone LeDoux et al, 1986a).…”

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Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear

et al. 1988

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The purpose of the present study was to determine whether lesions of areas projected to by the central amygdaloid nucleus (ACE) would disrupt the classical conditioning of autonomic and/or behavioral emotional responses. The areas studied included 3 projection targets of the ACE: the lateral hypothalamic area (LH), midbrain central gray (CG) region, and bed nucleus of the stria terminalis (BNST). Lesions were made either electrolytically or by microinjection of ibotenic acid, which destroys local neurons without interrupting fibers of passage. Two weeks later, the animals were classically conditioned by pairing an acoustic stimulus with footshock. The next day, conditioned changes in autonomic activity (increases in arterial pressure) and emotional behavior (“freezing,” or the arrest of somatomotor activity) evoked by the acoustic conditioned stimulus (CS) were measured during extinction trials. Electrolytic and ibotenic acid lesions of the LH interfered with the conditioned arterial pressure response, but did not affect conditioned freezing. Electrolytic lesions of the rostral CG disrupted conditioned freezing but not conditioned changes in arterial pressure. Ibotenic acid injected into the rostral CG reduced neither the arterial pressure nor the freezing response. Injection of ibotenic acid in the caudal CG, like electrolytic lesions of the rostral CG, disrupted the freezing, but not the arterial pressure response. Injection of ibotenic acid into the BNST had no effect on either response. These data demonstrate that neurons in the LH are involved in the autonomic, but not the behavioral, conditioned response pathway, whereas neurons in the caudal CG are involved in the behavioral, but not the autonomic, pathway. Different efferent projections of the central amygdala thus appear to mediate the behavioral and autonomic concomitants of conditioned fear.

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Intrinsic neurons in the amygdaloid field projected to by the medial geniculate body mediate emotional responses conditioned to acoustic stimuli

Cited by 268 publications

References 34 publications

Specific long-term memory traces in primary auditory cortex

Specific long-term memory traces in primary auditory cortex

Medial Geniculate Lesions Block Amygdalar and Cingulothalamic Learning-Related Neuronal Activity

Different projections of the central amygdaloid nucleus mediate autonomic and behavioral correlates of conditioned fear

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