Interruption of projections from the medial geniculate body to an archi-neostriatal field disrupts the classical conditioning of emotional responses to acoustic stimuli

Joseph Ledoux, A. Sakaguchi, J. Iwata, D. J. Reis

Research output: Contribution to journalArticle

Abstract

We have previously found that the coupling of changes in autonomie activity and emotional behavior to acoustic stimuli through classical fear conditioning survives bilateral ablation of auditory cortex but is disrupted by bilateral lesions of the medial geniculate nucleus or inferior colliculus in rats. Auditory fear conditioning thus appears to be mediated by the relay of acoustic input from the medial geniculate nucleus to subcortical rather than cortical targets. Since the medial geniculate nucleus projects, in addition to auditory cortex, to a striatal field, involving portions of the posterior neostriatum and underlying archistriatum (amygdala), we have sought to determine whether interruption of connections linking the medial geniculate nucleus to this subcortical field also disrupts conditioning. The conditioned emotional response model studied included the measurement of increases in mean arterial pressure and heart rate and the suppression of exploratory activity and drinking by the acoustic conditioned stimulus following delayed classical conditioning, where the footshock unconditioned stimulus appeared at the end of the conditioned stimulus. The peak increase in arterial pressure and the duration of activity and drinking suppression were greater in unoperated animals subjected to delayed conditioning than in pseudoconditioned controls, where the footshock was randomly rather than systematically related to the acoustic stimulus. Increases in heart rate, however, did not differ in conditioned and pseudoconditioned groups. While the arterial pressure and behavioral responses therefore reflect associative conditioning, the heart rate response does not. Rats were prepared with bilateral lesions of the medial geniculate nucleus, bilateral lesions of the striatal field or asymmetrical unilateral lesions destroying the medial geniculate nucleus on one side and the striatal field on the contralateral side. The latter preparation leaves one medial geniculate nucleus and one striatal field intact but disconnected and thus produces a selective auditory deafferentation of the intact striatal field. Control groups included animals with unilateral lesion of the medial geniculate nucleus, with unilateral lesion of the medial geniculate nucleus combined with lesion of the ipsilateral striatal field, unilateral lesion of the medial geniculate combined with lesion of the contralateral anterior neostriatum (a striatal area outside of the medial geniculate nucleus projection field), and the unilateral lesion of the medial geniculate nucleus combined with lesion of the contralateral ventromedial hypothalamus or subparafascicular thalamus (regions which receive projections from areas adjacent to the medial geniculate nucleus, but not from the medial geniculate nucleus itself). Bilateral lesions of the medial geniculate nucleus and bilateral lesions of the striatal field both drastically reduced the magnitude of the learned changes in arterial pressure and the duration of activity and drink suppression elicited by the conditioned stimulus. However, the nonassociative heart rate increase persisted. Asymmetric lesions involving one medial geniculate nucleus and the contralateral striatal field also disrupted the arterial pressure and behavioral, but not the heart rate, response. Lesions involving one medial geniculate nucleus and the ipsilateral striatal field did not disrupt any of the responses, nor did combined lesions involving one medial geniculate nucleus and the contralateral anterior neostriatum, ventromedial hypothalamus, or subparafascicular thalamus. Thus, bilateral destruction of either the medial geniculate nucleus or the striatal field or interruption of projections linking the medial geniculate nucleus to the striatal field disrupts associative changes in autonomie activity and behavior elicited by an acoustic conditioned stimulus. We conclude that auditory fear conditioning is mediated by efferent connections linking the medial geniculate nucleus to a striatal field, a subcortical projection field involving the posterior caudate-putamen (neostriatum) and/or amygdala (archistriatum). These connections are necessary for the establishment of associatively conditioned autonomie and somatomotor responses to an acoustic stimulus but do not appear to mediate nonassociative (pseudoconditioned) responses elicited by the same stimulus.

Original languageEnglish (US)
Pages (from-to)615-627
Number of pages13
JournalNeuroscience
Volume17
Issue number3
DOIs
StatePublished - 1986

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Geniculate Bodies
Classical Conditioning
Acoustics
Corpus Striatum
Neostriatum
Arterial Pressure
Amygdala
Heart Rate
Fear
Auditory Cortex
Thalamus
Hypothalamus
Drinking

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Interruption of projections from the medial geniculate body to an archi-neostriatal field disrupts the classical conditioning of emotional responses to acoustic stimuli. / Ledoux, Joseph; Sakaguchi, A.; Iwata, J.; Reis, D. J.

In: Neuroscience, Vol. 17, No. 3, 1986, p. 615-627.

Research output: Contribution to journalArticle

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abstract = "We have previously found that the coupling of changes in autonomie activity and emotional behavior to acoustic stimuli through classical fear conditioning survives bilateral ablation of auditory cortex but is disrupted by bilateral lesions of the medial geniculate nucleus or inferior colliculus in rats. Auditory fear conditioning thus appears to be mediated by the relay of acoustic input from the medial geniculate nucleus to subcortical rather than cortical targets. Since the medial geniculate nucleus projects, in addition to auditory cortex, to a striatal field, involving portions of the posterior neostriatum and underlying archistriatum (amygdala), we have sought to determine whether interruption of connections linking the medial geniculate nucleus to this subcortical field also disrupts conditioning. The conditioned emotional response model studied included the measurement of increases in mean arterial pressure and heart rate and the suppression of exploratory activity and drinking by the acoustic conditioned stimulus following delayed classical conditioning, where the footshock unconditioned stimulus appeared at the end of the conditioned stimulus. The peak increase in arterial pressure and the duration of activity and drinking suppression were greater in unoperated animals subjected to delayed conditioning than in pseudoconditioned controls, where the footshock was randomly rather than systematically related to the acoustic stimulus. Increases in heart rate, however, did not differ in conditioned and pseudoconditioned groups. While the arterial pressure and behavioral responses therefore reflect associative conditioning, the heart rate response does not. Rats were prepared with bilateral lesions of the medial geniculate nucleus, bilateral lesions of the striatal field or asymmetrical unilateral lesions destroying the medial geniculate nucleus on one side and the striatal field on the contralateral side. The latter preparation leaves one medial geniculate nucleus and one striatal field intact but disconnected and thus produces a selective auditory deafferentation of the intact striatal field. Control groups included animals with unilateral lesion of the medial geniculate nucleus, with unilateral lesion of the medial geniculate nucleus combined with lesion of the ipsilateral striatal field, unilateral lesion of the medial geniculate combined with lesion of the contralateral anterior neostriatum (a striatal area outside of the medial geniculate nucleus projection field), and the unilateral lesion of the medial geniculate nucleus combined with lesion of the contralateral ventromedial hypothalamus or subparafascicular thalamus (regions which receive projections from areas adjacent to the medial geniculate nucleus, but not from the medial geniculate nucleus itself). Bilateral lesions of the medial geniculate nucleus and bilateral lesions of the striatal field both drastically reduced the magnitude of the learned changes in arterial pressure and the duration of activity and drink suppression elicited by the conditioned stimulus. However, the nonassociative heart rate increase persisted. Asymmetric lesions involving one medial geniculate nucleus and the contralateral striatal field also disrupted the arterial pressure and behavioral, but not the heart rate, response. Lesions involving one medial geniculate nucleus and the ipsilateral striatal field did not disrupt any of the responses, nor did combined lesions involving one medial geniculate nucleus and the contralateral anterior neostriatum, ventromedial hypothalamus, or subparafascicular thalamus. Thus, bilateral destruction of either the medial geniculate nucleus or the striatal field or interruption of projections linking the medial geniculate nucleus to the striatal field disrupts associative changes in autonomie activity and behavior elicited by an acoustic conditioned stimulus. We conclude that auditory fear conditioning is mediated by efferent connections linking the medial geniculate nucleus to a striatal field, a subcortical projection field involving the posterior caudate-putamen (neostriatum) and/or amygdala (archistriatum). These connections are necessary for the establishment of associatively conditioned autonomie and somatomotor responses to an acoustic stimulus but do not appear to mediate nonassociative (pseudoconditioned) responses elicited by the same stimulus.",
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T1 - Interruption of projections from the medial geniculate body to an archi-neostriatal field disrupts the classical conditioning of emotional responses to acoustic stimuli

AU - Ledoux, Joseph

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AU - Reis, D. J.

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N2 - We have previously found that the coupling of changes in autonomie activity and emotional behavior to acoustic stimuli through classical fear conditioning survives bilateral ablation of auditory cortex but is disrupted by bilateral lesions of the medial geniculate nucleus or inferior colliculus in rats. Auditory fear conditioning thus appears to be mediated by the relay of acoustic input from the medial geniculate nucleus to subcortical rather than cortical targets. Since the medial geniculate nucleus projects, in addition to auditory cortex, to a striatal field, involving portions of the posterior neostriatum and underlying archistriatum (amygdala), we have sought to determine whether interruption of connections linking the medial geniculate nucleus to this subcortical field also disrupts conditioning. The conditioned emotional response model studied included the measurement of increases in mean arterial pressure and heart rate and the suppression of exploratory activity and drinking by the acoustic conditioned stimulus following delayed classical conditioning, where the footshock unconditioned stimulus appeared at the end of the conditioned stimulus. The peak increase in arterial pressure and the duration of activity and drinking suppression were greater in unoperated animals subjected to delayed conditioning than in pseudoconditioned controls, where the footshock was randomly rather than systematically related to the acoustic stimulus. Increases in heart rate, however, did not differ in conditioned and pseudoconditioned groups. While the arterial pressure and behavioral responses therefore reflect associative conditioning, the heart rate response does not. Rats were prepared with bilateral lesions of the medial geniculate nucleus, bilateral lesions of the striatal field or asymmetrical unilateral lesions destroying the medial geniculate nucleus on one side and the striatal field on the contralateral side. The latter preparation leaves one medial geniculate nucleus and one striatal field intact but disconnected and thus produces a selective auditory deafferentation of the intact striatal field. Control groups included animals with unilateral lesion of the medial geniculate nucleus, with unilateral lesion of the medial geniculate nucleus combined with lesion of the ipsilateral striatal field, unilateral lesion of the medial geniculate combined with lesion of the contralateral anterior neostriatum (a striatal area outside of the medial geniculate nucleus projection field), and the unilateral lesion of the medial geniculate nucleus combined with lesion of the contralateral ventromedial hypothalamus or subparafascicular thalamus (regions which receive projections from areas adjacent to the medial geniculate nucleus, but not from the medial geniculate nucleus itself). Bilateral lesions of the medial geniculate nucleus and bilateral lesions of the striatal field both drastically reduced the magnitude of the learned changes in arterial pressure and the duration of activity and drink suppression elicited by the conditioned stimulus. However, the nonassociative heart rate increase persisted. Asymmetric lesions involving one medial geniculate nucleus and the contralateral striatal field also disrupted the arterial pressure and behavioral, but not the heart rate, response. Lesions involving one medial geniculate nucleus and the ipsilateral striatal field did not disrupt any of the responses, nor did combined lesions involving one medial geniculate nucleus and the contralateral anterior neostriatum, ventromedial hypothalamus, or subparafascicular thalamus. Thus, bilateral destruction of either the medial geniculate nucleus or the striatal field or interruption of projections linking the medial geniculate nucleus to the striatal field disrupts associative changes in autonomie activity and behavior elicited by an acoustic conditioned stimulus. We conclude that auditory fear conditioning is mediated by efferent connections linking the medial geniculate nucleus to a striatal field, a subcortical projection field involving the posterior caudate-putamen (neostriatum) and/or amygdala (archistriatum). These connections are necessary for the establishment of associatively conditioned autonomie and somatomotor responses to an acoustic stimulus but do not appear to mediate nonassociative (pseudoconditioned) responses elicited by the same stimulus.

AB - We have previously found that the coupling of changes in autonomie activity and emotional behavior to acoustic stimuli through classical fear conditioning survives bilateral ablation of auditory cortex but is disrupted by bilateral lesions of the medial geniculate nucleus or inferior colliculus in rats. Auditory fear conditioning thus appears to be mediated by the relay of acoustic input from the medial geniculate nucleus to subcortical rather than cortical targets. Since the medial geniculate nucleus projects, in addition to auditory cortex, to a striatal field, involving portions of the posterior neostriatum and underlying archistriatum (amygdala), we have sought to determine whether interruption of connections linking the medial geniculate nucleus to this subcortical field also disrupts conditioning. The conditioned emotional response model studied included the measurement of increases in mean arterial pressure and heart rate and the suppression of exploratory activity and drinking by the acoustic conditioned stimulus following delayed classical conditioning, where the footshock unconditioned stimulus appeared at the end of the conditioned stimulus. The peak increase in arterial pressure and the duration of activity and drinking suppression were greater in unoperated animals subjected to delayed conditioning than in pseudoconditioned controls, where the footshock was randomly rather than systematically related to the acoustic stimulus. Increases in heart rate, however, did not differ in conditioned and pseudoconditioned groups. While the arterial pressure and behavioral responses therefore reflect associative conditioning, the heart rate response does not. Rats were prepared with bilateral lesions of the medial geniculate nucleus, bilateral lesions of the striatal field or asymmetrical unilateral lesions destroying the medial geniculate nucleus on one side and the striatal field on the contralateral side. The latter preparation leaves one medial geniculate nucleus and one striatal field intact but disconnected and thus produces a selective auditory deafferentation of the intact striatal field. Control groups included animals with unilateral lesion of the medial geniculate nucleus, with unilateral lesion of the medial geniculate nucleus combined with lesion of the ipsilateral striatal field, unilateral lesion of the medial geniculate combined with lesion of the contralateral anterior neostriatum (a striatal area outside of the medial geniculate nucleus projection field), and the unilateral lesion of the medial geniculate nucleus combined with lesion of the contralateral ventromedial hypothalamus or subparafascicular thalamus (regions which receive projections from areas adjacent to the medial geniculate nucleus, but not from the medial geniculate nucleus itself). Bilateral lesions of the medial geniculate nucleus and bilateral lesions of the striatal field both drastically reduced the magnitude of the learned changes in arterial pressure and the duration of activity and drink suppression elicited by the conditioned stimulus. However, the nonassociative heart rate increase persisted. Asymmetric lesions involving one medial geniculate nucleus and the contralateral striatal field also disrupted the arterial pressure and behavioral, but not the heart rate, response. Lesions involving one medial geniculate nucleus and the ipsilateral striatal field did not disrupt any of the responses, nor did combined lesions involving one medial geniculate nucleus and the contralateral anterior neostriatum, ventromedial hypothalamus, or subparafascicular thalamus. Thus, bilateral destruction of either the medial geniculate nucleus or the striatal field or interruption of projections linking the medial geniculate nucleus to the striatal field disrupts associative changes in autonomie activity and behavior elicited by an acoustic conditioned stimulus. We conclude that auditory fear conditioning is mediated by efferent connections linking the medial geniculate nucleus to a striatal field, a subcortical projection field involving the posterior caudate-putamen (neostriatum) and/or amygdala (archistriatum). These connections are necessary for the establishment of associatively conditioned autonomie and somatomotor responses to an acoustic stimulus but do not appear to mediate nonassociative (pseudoconditioned) responses elicited by the same stimulus.

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