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The amygdala: Neurobiological aspects of emotion, memory and mental dysfunction
J o u r n a l of Chemical N e u r o a n a t o m y , Vol. 6:331 334 (1993)
Book Reviews The Amygdala: Neurobiological Aspects of Emotion, Memory and Mental Dysfunction John P. Aggleton (editor). Wiley-Liss, Inc., 1992. £98/$1 47. This book follows the fine tradition of publishing each decade a new book dedicated to review our current knowledge of the amygdaloid complex. The first books represent publications of scientific meetings: the first volume, edited by Eleftherion (1972), was entitled The Neurobiology of the Amygdala and the second volume, by Ben-Ari (1982), The Amygdaloid Complex. The present book, edited by J. P. Aggleton (1992), represents a major contribution to our current understanding of the amygdala. The book contains 23 chapters by selected and leading scientists within the fields of neuroanatomy, neurochemistry, electrophysiology and behavioural studies. Some chapters concentrate on the involvement of the amygdala in various clinical conditions. It seems obvious that the amygdaloid complex is involved in the advanced processing of sensory information from the level of unisensori and polysensori cortical association areas, the thalamus, and direct impulses from autonomic and visceral brain stem and hypothalamic centres. A main function of the amygdala is to provide the "appropriate affective bias" or "mood' evoked by environmental stimuli, to which the organism is exposed. A lesion or a chemical activation of the amygdaloid complex induces an inability ('psychic blindness') to relate environmental signals into the normal adaptive behavioural response. Weiskrantz (1956) and later Geschwind (1965) and Mishkin and Jones (1972), based on their analyses on the Kliiver-Bucy syndrome, concluded that sensory stimuli processed in the temporal lobe must interact with the amygdala in order to be established with the appropriate affective and motivational significance. In several chapters this original framework forms the basis for reviews on the role of the amygdala in anxiety, fear, attention, learning and memory, social behaviour and goal-directed behaviour. The scene is already set in the introductory chapter by Amaral, Price et al., who cover the anatomical background on the myriads of routes by which the primate amygdaloid complex can affect and/or modulate behaviour and sensory processing related to widespread regions of the brain. Major emphasis should be paid to the efferent projections from the monkey amygdala (basal nucleus), which are directed towards the cortex and the striatal system. This chapter is also focussed on the interaction between the two major structures in the limbic system. The monkey amygdala is anatomically in a position to have a substantially greater influence on the hippocampal formarion than vice versa. This seems to be essential, since the hippocampus, via the entorhinal cortex, also receives major afferent/efferent connections with all the major and higher cortical association areas. The hippocampal ~) 1993 by J o h n Wiley a n d Sons Ltd
formation thus represents a supra-modal sensory processing unit with the ability to form new declarative or episodic memories. The distribution of all known neurotransmitters and peptides in the primate amygdala is summarized. However, the progressive phylogenetic development of particularly the lateral, basal and accessory basal complex still represents a problem for the exact homologies in lower animal species; i.e. in the rat the 'basolateral complex' can still be seen in the nomenclature in several chapters. The chapters on anatomy, cell types, intrinsic connections and the distribution of the monoamines in the rat are presented by McDonald, Fallon and Roberts. It seems that the monoamines and virtually all neuropeptides found in the brain can be localized to various cells or fibres within the amygdaloid complex. It is unfortunate that the summary wiring diagram by McDonald on the extrinsic/intrinsicconnections (Fig. 10) does not exactly agree with Amaral et al. and Le Doux (chapter 12). There are also inconsistenciesconcerning the important issue that the afferent integration from cortex and thalamus takes place in the lateral nucleus belk~re one or more stages of intrinsic processing to the basal nucleus, which projects extensively back to the cortex iAmaral, Fig. 8). Unfortunately, all anatomical chapters lack a current and/or hypothetical wiring diagram on the synaptic organization between the excitatory/inhibitory afferent and efferent connections of the amygdala. Today, we do know that both the principal pyramidal (glutamate) type I and the type It (gamma-aminobutyric acid (GABA)-ergic interneurons) with the lateral and basal amygdaloid complex receive both excitatory and inhibitory inputs from the hippocampal formation and the basal forebrain (GABA, acetylcholine). The chapters by Davis, Gallagher, Henke, Kapp et al. and Le Doux represent a series of excellent, often complementary, studies summarizing our current knowledge of the amygdala as a nodal area of the brain l\~r the acquisition and expression of anxiety, stress, arousal, conditioned fear and emotions. The central nucleus of the amygdala with its substantial amount of afferent/efferent connections represents a critical component in the forebrain for associative learning. The anatomical studies link the central nucleus to inputs of events (conditioned or unconditioned stimuli) that may serve the basis for learning and also for several substantial output systems for the expression of visceral, autonomic, unconditioned/reflexiveand voluntary behavioural acts. It was also fascinating to learn about all the possible levels at which the amygdala is potentially able to contribute to arousal and attention processes via its activating effects in the brain stem of autonomic nuclei, the noradrenaline system and the ascending cholinergic system
332
B o o k Reviews
from the latero-dorsal nuclei innervating the thalamus, the magnocellular cholinergic neurons in the basal forebrain innervating the cortex. The amygdala thus represents a nodal structure for sensory information processing, as Haigren speculates 'a metaphor for the connection of mind and body'. Future research may determine the way in which sensory information is gated into the phylogenetic progression from reptiles to man, and how, during normal circumstances, the amygdala may produce the emotional lift of enjoying life, the opposite sex, listening to music, and soon, and how the balance may be disturbed during extreme or pathological clinical conditions. The substantial amounts of neurotransmitters/neuropeptides within the amygdala undoubtedly contribute to adapt neuronal plasticity to new challenges. The chapters on stimulus-reinforcement association present excellent discussions on the intimate functional interaction between the cortical regions of the temporal and orbital cortical regions (Rolls, Gaffan). I noticed in particular the possible role of the back-projections from the amygdala to the temporal neocortex as a guidance of stimuli representation and long-term storage of biological (novel) significant reinforcing stimuli (positive or negative), their role for later recall and the significance of the orbital frontal cortex for rapid switching or reversals of changing reinforcement conditions. The rhinal cortex in the ventromedial temporal lobe is frequently lesioned in primate experiments intended for the amygdala or hippocampal structures, but this cortical region is now considered to contribute critically to recognition memory (Murray). In the rat amygdala, the encoding and memory formation seems particularly striking under conditions of a sufficient intensity of reinforcement for eliciting emotional reactions, arousal and autonomic changes (Kesner, McGaugh). Ono et al. presented the functional electrophysiology on the temporal cortical-amygdala link to the lateral hypothalamus in the reward-output system. Everitt and Robbins contributed by discussing the role of the baso-
lateral amygdala and the mesolimbic dopamine system localized to the nucleus accumbens as the neural structures involved in the expression of the motor elements of reward-related processes. The final chapters (Aggleton, Gloor, Cain, Kling, Reynolds) present functional aspects of amygdala lesions or dysfunctions in humans in temporal lope epilepsy, kindling, schizophrenia, and the neuropathology of the amygdala in ageing and dementia (Mann). I was surprised that this book did not contain a chapter on the current status of the amygdala and depression. However, this topic was certainly in focus in a recent book entitled The Mesolimbic Dopamine System: From Motivation to Action (eds P. Willner and J. ScheeI-Krfiger, 1991, J. Wiley & Sons), in which the mesolimbic dopamine system, and the role of the nucleus accumbens, were discussed to a large extent according to Mogenson's concept as the functional interphase for the mutual interaction between the major limbic structures, the hippocampus and the amygdala. I think that this book should also have included a section on 'the extended amygdaloid complex' of Alheid and Heimer (1988) involving the basal forebrain. This book is well written and contains only a few typographical errors. It was a pleasure to read it, and a substantial amount of new information has been accumulated since the last book published a decade ago. It now seems appropriate not only to consider the amygdala as a sensory gateway to emotions (Aggleton and Mishkin, 1986), but also to extend the status of this important structure as a gateway for our understanding of the functions of the limbic system. The involvement of the amygdala in attention, emotion, motiviation, learning and memory becomes obvious.
Jgrgen Seheel-Kriiger Department of Psychopharmacology NeuroSearch A/S Smedeland 26 DK2600 GIostrup Denmark
Functional Anatomy of the Neuroendocrine Hypothalamus Edited by D. J. Chadwick and J. M a r s h Published by J o h n Wiley and Sons, Chichester, as volume 168 o f the C I B A F o u n d a t i o n Symposium series ( I S B N 0 471 93440 2) This book contains the proceedings of a meeting held in Budapest in October 1991 under the same title, and consists of 16 contributions of an international panel of experts on the subject. In addition to the standard of the contributions, the scientific value of the book is certainly boosted by the reports of the discussions that followed each of the presentations. These discussion reports comprise approximately one third of the total volume of this publication and contain explicit references to published work. Often, they contain refreshing views that can be expected from an audience consisting of experts, all having their own history of scientific successes and fustrations. The book is focussed on fundamental aspects of hypothalamic functioning rather than on clinical implications, as stated by S. L. Lightman in his introduction. Accordingly, most of the experimental findings presented here are derived from studies with experimental animals or cells.
Although the format of this series puts limitations on the number of contributors and thereby on the number of topics covered, I feel that the book gives a interesting overview of the state of the art in this particular field. In this publication, the 'neuroendocrine hypothalamus 'refers primarily to those cells, nuclei and neuronal networks that are responsible for the production, storage and secretion of hypophysiotropic signals and thereby to those cells that are directly involved in the control of specific functions of the pituitary gland. A recurrent theme is that the generation of physiologically relevant hypophysiotropic signals requires coordination of the secretory activity of a given set of neurons. Synchronization of secretory activity may be an intrinsic property of intercellular communication between a given group of peptidergic neurons. In support of this, the majority of the synapses found in the paraventricular and supraoptic nuclei were reported to be intrinsic, i.e. originate from
Book Reviews The Amygdala: Neurobiological Aspects of Emotion, Memory and Mental Dysfunction John P. Aggleton (editor). Wiley-Liss, Inc., 1992. £98/$1 47. This book follows the fine tradition of publishing each decade a new book dedicated to review our current knowledge of the amygdaloid complex. The first books represent publications of scientific meetings: the first volume, edited by Eleftherion (1972), was entitled The Neurobiology of the Amygdala and the second volume, by Ben-Ari (1982), The Amygdaloid Complex. The present book, edited by J. P. Aggleton (1992), represents a major contribution to our current understanding of the amygdala. The book contains 23 chapters by selected and leading scientists within the fields of neuroanatomy, neurochemistry, electrophysiology and behavioural studies. Some chapters concentrate on the involvement of the amygdala in various clinical conditions. It seems obvious that the amygdaloid complex is involved in the advanced processing of sensory information from the level of unisensori and polysensori cortical association areas, the thalamus, and direct impulses from autonomic and visceral brain stem and hypothalamic centres. A main function of the amygdala is to provide the "appropriate affective bias" or "mood' evoked by environmental stimuli, to which the organism is exposed. A lesion or a chemical activation of the amygdaloid complex induces an inability ('psychic blindness') to relate environmental signals into the normal adaptive behavioural response. Weiskrantz (1956) and later Geschwind (1965) and Mishkin and Jones (1972), based on their analyses on the Kliiver-Bucy syndrome, concluded that sensory stimuli processed in the temporal lobe must interact with the amygdala in order to be established with the appropriate affective and motivational significance. In several chapters this original framework forms the basis for reviews on the role of the amygdala in anxiety, fear, attention, learning and memory, social behaviour and goal-directed behaviour. The scene is already set in the introductory chapter by Amaral, Price et al., who cover the anatomical background on the myriads of routes by which the primate amygdaloid complex can affect and/or modulate behaviour and sensory processing related to widespread regions of the brain. Major emphasis should be paid to the efferent projections from the monkey amygdala (basal nucleus), which are directed towards the cortex and the striatal system. This chapter is also focussed on the interaction between the two major structures in the limbic system. The monkey amygdala is anatomically in a position to have a substantially greater influence on the hippocampal formarion than vice versa. This seems to be essential, since the hippocampus, via the entorhinal cortex, also receives major afferent/efferent connections with all the major and higher cortical association areas. The hippocampal ~) 1993 by J o h n Wiley a n d Sons Ltd
formation thus represents a supra-modal sensory processing unit with the ability to form new declarative or episodic memories. The distribution of all known neurotransmitters and peptides in the primate amygdala is summarized. However, the progressive phylogenetic development of particularly the lateral, basal and accessory basal complex still represents a problem for the exact homologies in lower animal species; i.e. in the rat the 'basolateral complex' can still be seen in the nomenclature in several chapters. The chapters on anatomy, cell types, intrinsic connections and the distribution of the monoamines in the rat are presented by McDonald, Fallon and Roberts. It seems that the monoamines and virtually all neuropeptides found in the brain can be localized to various cells or fibres within the amygdaloid complex. It is unfortunate that the summary wiring diagram by McDonald on the extrinsic/intrinsicconnections (Fig. 10) does not exactly agree with Amaral et al. and Le Doux (chapter 12). There are also inconsistenciesconcerning the important issue that the afferent integration from cortex and thalamus takes place in the lateral nucleus belk~re one or more stages of intrinsic processing to the basal nucleus, which projects extensively back to the cortex iAmaral, Fig. 8). Unfortunately, all anatomical chapters lack a current and/or hypothetical wiring diagram on the synaptic organization between the excitatory/inhibitory afferent and efferent connections of the amygdala. Today, we do know that both the principal pyramidal (glutamate) type I and the type It (gamma-aminobutyric acid (GABA)-ergic interneurons) with the lateral and basal amygdaloid complex receive both excitatory and inhibitory inputs from the hippocampal formation and the basal forebrain (GABA, acetylcholine). The chapters by Davis, Gallagher, Henke, Kapp et al. and Le Doux represent a series of excellent, often complementary, studies summarizing our current knowledge of the amygdala as a nodal area of the brain l\~r the acquisition and expression of anxiety, stress, arousal, conditioned fear and emotions. The central nucleus of the amygdala with its substantial amount of afferent/efferent connections represents a critical component in the forebrain for associative learning. The anatomical studies link the central nucleus to inputs of events (conditioned or unconditioned stimuli) that may serve the basis for learning and also for several substantial output systems for the expression of visceral, autonomic, unconditioned/reflexiveand voluntary behavioural acts. It was also fascinating to learn about all the possible levels at which the amygdala is potentially able to contribute to arousal and attention processes via its activating effects in the brain stem of autonomic nuclei, the noradrenaline system and the ascending cholinergic system
332
B o o k Reviews
from the latero-dorsal nuclei innervating the thalamus, the magnocellular cholinergic neurons in the basal forebrain innervating the cortex. The amygdala thus represents a nodal structure for sensory information processing, as Haigren speculates 'a metaphor for the connection of mind and body'. Future research may determine the way in which sensory information is gated into the phylogenetic progression from reptiles to man, and how, during normal circumstances, the amygdala may produce the emotional lift of enjoying life, the opposite sex, listening to music, and soon, and how the balance may be disturbed during extreme or pathological clinical conditions. The substantial amounts of neurotransmitters/neuropeptides within the amygdala undoubtedly contribute to adapt neuronal plasticity to new challenges. The chapters on stimulus-reinforcement association present excellent discussions on the intimate functional interaction between the cortical regions of the temporal and orbital cortical regions (Rolls, Gaffan). I noticed in particular the possible role of the back-projections from the amygdala to the temporal neocortex as a guidance of stimuli representation and long-term storage of biological (novel) significant reinforcing stimuli (positive or negative), their role for later recall and the significance of the orbital frontal cortex for rapid switching or reversals of changing reinforcement conditions. The rhinal cortex in the ventromedial temporal lobe is frequently lesioned in primate experiments intended for the amygdala or hippocampal structures, but this cortical region is now considered to contribute critically to recognition memory (Murray). In the rat amygdala, the encoding and memory formation seems particularly striking under conditions of a sufficient intensity of reinforcement for eliciting emotional reactions, arousal and autonomic changes (Kesner, McGaugh). Ono et al. presented the functional electrophysiology on the temporal cortical-amygdala link to the lateral hypothalamus in the reward-output system. Everitt and Robbins contributed by discussing the role of the baso-
lateral amygdala and the mesolimbic dopamine system localized to the nucleus accumbens as the neural structures involved in the expression of the motor elements of reward-related processes. The final chapters (Aggleton, Gloor, Cain, Kling, Reynolds) present functional aspects of amygdala lesions or dysfunctions in humans in temporal lope epilepsy, kindling, schizophrenia, and the neuropathology of the amygdala in ageing and dementia (Mann). I was surprised that this book did not contain a chapter on the current status of the amygdala and depression. However, this topic was certainly in focus in a recent book entitled The Mesolimbic Dopamine System: From Motivation to Action (eds P. Willner and J. ScheeI-Krfiger, 1991, J. Wiley & Sons), in which the mesolimbic dopamine system, and the role of the nucleus accumbens, were discussed to a large extent according to Mogenson's concept as the functional interphase for the mutual interaction between the major limbic structures, the hippocampus and the amygdala. I think that this book should also have included a section on 'the extended amygdaloid complex' of Alheid and Heimer (1988) involving the basal forebrain. This book is well written and contains only a few typographical errors. It was a pleasure to read it, and a substantial amount of new information has been accumulated since the last book published a decade ago. It now seems appropriate not only to consider the amygdala as a sensory gateway to emotions (Aggleton and Mishkin, 1986), but also to extend the status of this important structure as a gateway for our understanding of the functions of the limbic system. The involvement of the amygdala in attention, emotion, motiviation, learning and memory becomes obvious.
Jgrgen Seheel-Kriiger Department of Psychopharmacology NeuroSearch A/S Smedeland 26 DK2600 GIostrup Denmark
Functional Anatomy of the Neuroendocrine Hypothalamus Edited by D. J. Chadwick and J. M a r s h Published by J o h n Wiley and Sons, Chichester, as volume 168 o f the C I B A F o u n d a t i o n Symposium series ( I S B N 0 471 93440 2) This book contains the proceedings of a meeting held in Budapest in October 1991 under the same title, and consists of 16 contributions of an international panel of experts on the subject. In addition to the standard of the contributions, the scientific value of the book is certainly boosted by the reports of the discussions that followed each of the presentations. These discussion reports comprise approximately one third of the total volume of this publication and contain explicit references to published work. Often, they contain refreshing views that can be expected from an audience consisting of experts, all having their own history of scientific successes and fustrations. The book is focussed on fundamental aspects of hypothalamic functioning rather than on clinical implications, as stated by S. L. Lightman in his introduction. Accordingly, most of the experimental findings presented here are derived from studies with experimental animals or cells.
Although the format of this series puts limitations on the number of contributors and thereby on the number of topics covered, I feel that the book gives a interesting overview of the state of the art in this particular field. In this publication, the 'neuroendocrine hypothalamus 'refers primarily to those cells, nuclei and neuronal networks that are responsible for the production, storage and secretion of hypophysiotropic signals and thereby to those cells that are directly involved in the control of specific functions of the pituitary gland. A recurrent theme is that the generation of physiologically relevant hypophysiotropic signals requires coordination of the secretory activity of a given set of neurons. Synchronization of secretory activity may be an intrinsic property of intercellular communication between a given group of peptidergic neurons. In support of this, the majority of the synapses found in the paraventricular and supraoptic nuclei were reported to be intrinsic, i.e. originate from