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

Jiro Iwata, Joseph Ledoux, Mary P. Meeley, Stephen Arneric, Donald J. Reis

Research output: Contribution to journalArticle

Abstract

In previous experiments we implicated projections from the medial geniculate body (MG) to a subcortical field, involving portions of the posterior caudate-putamen and amygdala, in the classical conditioning of emotional responses to acoustic stimuli in the rat. In the present series of experiments we examined whether intrinsic neurons in the subcortical field mediate emotional conditioning and, if so, whether the critical neurons are contained within the amygdala or the caudate-putamen. Rats were prepared with a unilateral electrolytic lesion of the MG. Contralaterally, intrinsic neurons were destroyed in the subcortical field by microinjection of ibotenic acid. This lesion combination leaves one MG and one subcortical field intact but disconnected. Controls received unilateral injection of phosphate buffer vehicle into the subcortical field contralateral to the MG lesion or were unoperated. After two weeks the animals were instrumented for continuous, computer-assisted recording of arterial pressure and heart rate and subjected to classical conditioning trials involving the presentation of a pure tone in association with foot-shock. The occurrence of the shock with respect to the tone was random for a pseudoconditioned control group. Conditioned changes in mean arterial pressure, heart rate and emotional behavior ('freezing') elicited by the tone were assessed during extinction trials. Following completion of the experiments, the rats were sacrificed and their brains were removed and sectioned using standard procedures. Lesion location and size was evaluated with the assistance of a computer-based image processing system. In unoperated conditioned rats the acoustic stimulus elicited increases in arterial pressure and heart rate, and induced freezing. The arterial pressure and freezing responses differed in conditioned and pseudoconditioned rats, but the heart rate response did not. Therefore, only the arterial pressure and freezing responses reflect the formation of an association between the tone and shock. Destruction of intrinsic neurons in the subcortical field contralateral to a unilateral MG lesion disrupted the associative conditioning of the arterial pressure and freezing responses. These were reduced in magnitude to the level observed in pseudoconditioned rats. The non-associative heart rate change was not affected by the lesions. That ibotenic acid destroyed intrinsic neurons and spared fibers in the subcortical field was demonstrated anatomically and biochemically. Thus, intrinsic neurons in the subcortical field innervated by the MG appear to mediate associative emotional conditioning. To determine whether the critical associative neurons are contained within the amygdala or caudate-putamen, additional animals were prepared with a unilateral MG lesion combined with injection of ibotenic acid contralaterally in either the posterior caudate-putamen or the amygdala. Caudate-putamen injections had no effect on any of the responses. In contrast, amygdala injections either disrupted both arterial pressure and freezing responses, disrupted only freezing, or had no effect on either. Amygdala injections did not reduce the heart rate changes. Those cell lesions of the amygdala which had no effect were significantly smaller than the lesions which disrupted one or both responses. The area of cell loss in the subgroup in which both responses were disrupted consistently involved the fundus striati (the putamen part of the amygdala) and the underlying central nucleus of the amygdala. The lesions disrupting only freezing responses were centered in the lateral nucleus and the lateral part of the central nucleus of the amygdala. The ineffective lesions were not consistently localized in any one region. In summary, selective destruction of intrinsic neurons within the amygdaloid field innervated by the MG disrupts associative emotional conditioning. The coupling of emotional significance to acoustic stimuli may, therefore, involve the relay of sensory input from the MG to the amygdala.

Original languageEnglish (US)
Pages (from-to)195-214
Number of pages20
JournalBrain Research
Volume383
Issue number1-2
DOIs
StatePublished - Sep 24 1986

Fingerprint

Geniculate Bodies
Amygdala
Acoustics
Freezing
Putamen
Neurons
Arterial Pressure
Heart Rate
Ibotenic Acid
Injections
Shock
Classical Conditioning
Microinjections
Foot
Buffers
Phosphates
Control Groups

Keywords

  • Amygdala
  • Classical conditioning
  • Emotion
  • Medial geniculate body

ASJC Scopus subject areas

  • Developmental Biology
  • Molecular Biology
  • Clinical Neurology
  • Neuroscience(all)

Cite this

Intrinsic neurons in the amygdaloid field projected to by the medial geniculate body mediate emotional responses conditioned to acoustic stimuli. / Iwata, Jiro; Ledoux, Joseph; Meeley, Mary P.; Arneric, Stephen; Reis, Donald J.

In: Brain Research, Vol. 383, No. 1-2, 24.09.1986, p. 195-214.

Research output: Contribution to journalArticle

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AU - Ledoux, Joseph

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AU - Arneric, Stephen

AU - Reis, Donald J.

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N2 - In previous experiments we implicated projections from the medial geniculate body (MG) to a subcortical field, involving portions of the posterior caudate-putamen and amygdala, in the classical conditioning of emotional responses to acoustic stimuli in the rat. In the present series of experiments we examined whether intrinsic neurons in the subcortical field mediate emotional conditioning and, if so, whether the critical neurons are contained within the amygdala or the caudate-putamen. Rats were prepared with a unilateral electrolytic lesion of the MG. Contralaterally, intrinsic neurons were destroyed in the subcortical field by microinjection of ibotenic acid. This lesion combination leaves one MG and one subcortical field intact but disconnected. Controls received unilateral injection of phosphate buffer vehicle into the subcortical field contralateral to the MG lesion or were unoperated. After two weeks the animals were instrumented for continuous, computer-assisted recording of arterial pressure and heart rate and subjected to classical conditioning trials involving the presentation of a pure tone in association with foot-shock. The occurrence of the shock with respect to the tone was random for a pseudoconditioned control group. Conditioned changes in mean arterial pressure, heart rate and emotional behavior ('freezing') elicited by the tone were assessed during extinction trials. Following completion of the experiments, the rats were sacrificed and their brains were removed and sectioned using standard procedures. Lesion location and size was evaluated with the assistance of a computer-based image processing system. In unoperated conditioned rats the acoustic stimulus elicited increases in arterial pressure and heart rate, and induced freezing. The arterial pressure and freezing responses differed in conditioned and pseudoconditioned rats, but the heart rate response did not. Therefore, only the arterial pressure and freezing responses reflect the formation of an association between the tone and shock. Destruction of intrinsic neurons in the subcortical field contralateral to a unilateral MG lesion disrupted the associative conditioning of the arterial pressure and freezing responses. These were reduced in magnitude to the level observed in pseudoconditioned rats. The non-associative heart rate change was not affected by the lesions. That ibotenic acid destroyed intrinsic neurons and spared fibers in the subcortical field was demonstrated anatomically and biochemically. Thus, intrinsic neurons in the subcortical field innervated by the MG appear to mediate associative emotional conditioning. To determine whether the critical associative neurons are contained within the amygdala or caudate-putamen, additional animals were prepared with a unilateral MG lesion combined with injection of ibotenic acid contralaterally in either the posterior caudate-putamen or the amygdala. Caudate-putamen injections had no effect on any of the responses. In contrast, amygdala injections either disrupted both arterial pressure and freezing responses, disrupted only freezing, or had no effect on either. Amygdala injections did not reduce the heart rate changes. Those cell lesions of the amygdala which had no effect were significantly smaller than the lesions which disrupted one or both responses. The area of cell loss in the subgroup in which both responses were disrupted consistently involved the fundus striati (the putamen part of the amygdala) and the underlying central nucleus of the amygdala. The lesions disrupting only freezing responses were centered in the lateral nucleus and the lateral part of the central nucleus of the amygdala. The ineffective lesions were not consistently localized in any one region. In summary, selective destruction of intrinsic neurons within the amygdaloid field innervated by the MG disrupts associative emotional conditioning. The coupling of emotional significance to acoustic stimuli may, therefore, involve the relay of sensory input from the MG to the amygdala.

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