The human amygdala

452 Pages·2009·6.783 MB·English

by  Phelps, Elizabeth A., Whalen, Paul J

The human
amygdala

ediTed by
Paul J. Whalen
elizabeTh a. PhelPs
The guilFORd PRess
new york london
Contents
Part I. From Animal Models
to Human Amygdala Function
ChapTer 1. neuroanatomy of the Primate amygdala 3
Jennifer L. Freese and David G. Amaral
ChapTer 2. The human amygdala: insights from Other animals 43
Joseph E. LeDoux and Daniela Schiller
ChapTer 3. measurement of Fear inhibition in Rats, monkeys, 61
and humans with or without Posttraumatic stress
disorder, using the aX+, bX– Paradigm
Karyn M. Myers, Donna J. Toufexis, James T. Winslow,
Tanja Jovanovic, Seth D. Norrholm, Erica J. Duncan,
and Michael Davis
ChapTer 4. amygdala Function in Positive Reinforcement: 82
Contributions from studies of nonhuman Primates
Elisabeth A. Murray, Alicia Izquierdo, and Ludise Malkova
Part II. Human Amygdala Function
ChapTer 5. a developmental Perspective on human 107
amygdala Function
Nim Tottenham, Todd A. Hare, and B. J. Casey
ChapTer 6. human Fear Conditioning and the amygdala 118
Arne Öhman
xiii
xiv Contents
ChapTer 7. methodological approaches to studying 155
the human amygdala
Kevin S. LaBar and Lauren H. Warren
ChapTer 8. The human amygdala and memory 177
Stephan Hamann
ChapTer 9. The human amygdala and the Control of Fear 204
Elizabeth A. Phelps
ChapTer 10. The Role of the human amygdala in Perception 220
and attention
Patrik Vuilleumier
ChapTer 11. individual differences in human amygdala Function 250
Turhan Canli
ChapTer 12. human amygdala Responses to Facial expressions 265
of emotion
Paul J. Whalen, F. Caroline Davis, Jonathan A. Oler,
Hackjin Kim, M. Justin Kim, and Maital Neta
ChapTer 13. The human amygdala in social Function 289
Tony W. Buchanan, Daniel Tranel, and Ralph Adolphs
Part III. Human Amygdala Dysfunction
ChapTer 14. The human amygdala in anxiety disorders 321
Lisa M. Shin, Scott L. Rauch, Roger K. Pitman,
and Paul J. Whalen
ChapTer 15. The human amygdala in schizophrenia 344
Daphne J. Holt and Mary L. Phillips
ChapTer 16. The human amygdala in autism 362
Cynthia Mills Schumann and David G. Amaral
ChapTer 17. The human amygdala in normal aging 382
and alzheimer’s disease
Christopher I. Wright
ChapTer 18. The genetic basis of amygdala Reactivity 406
Ahmad R. Hariri and Daniel R. Weinberger
index 417
PaRT i
From Animal Models
to Human Amygdala Function

ChapTer 1
neuroanatomy of the Primate amygdala
Jennifer L. Freese and David G. Amaral
The amygdala1 has historically been considered to be part of the limbic sys-
tem, with connections mainly to the hypothalamus and brainstem. How-
ever, neuroanatomical studies carried out over the last 30 years clearly
demonstrate that the amygdala has a wide- reaching network of connections
with a diverse array of brain regions (Aggleton, Burton, & Passingham, 1980;
Aggleton & Mishkin, 1984; Amaral & Price, 1984; Amaral, Price, Pitkänen,
& Carmichael, 1992; Amaral, Veazey, & Cowan, 1982; Carmichael & Price,
1995; Cheng et al., 1997; Freese & Amaral, 2005; Fudge, Kunishio, Walsh,
Richard, & Haber, 2002; Iwai & Yukie, 1987; Mehler, 1980; Mizuno, Taka-
hashi, Satoda, & Matsushima, 1985; Norita & Kawamura, 1980; Russchen,
Bakst, Amaral, & Price, 1985). Moreover, it is also clear that the amygdala
has undergone an evolutionary reorganization; for example, the lateral nucleus
of the amygdala occupies a much larger proportion of the nonhuman primate
and human amygdala than of the rodent or carnivore amygdala (Barger, Stefa-
nacci, & Semendeferi, 2007; Stephan, Frahm, & Baron, 1987). This makes
sense, given that the lateral nucleus is the major recipient of neocortical inputs,
and the neocortex has undergone the greatest elaboration in the primate brain
(Gloor, 1997; McDonald, 1998; Stephan et al., 1987).
The neuroanatomy of the amygdaloid complex has been reviewed on a
number of occasions over the last 30 years (Aggleton et al., 1980; Amaral
et al., 1992; McDonald, 1992; Price, Russchen, & Amaral, 1987). In this
short chapter, we focus on a description of the subdivisions and patterns of
connectivity of the nonhuman primate amygdaloid complex. Available evi-
3
4 FROm animal mOdels TO human amygdala FunCTiOn
dence indicates that the macaque monkey amygdala is a reasonable proxy
for the human amygdala. Where comparisons have been made—for exam-
ple, in the cytoarchitectonic organization (Pitkänen & Kemppainen, 2002;
Sorvari, Soininen, Palijarvi, Karkola, & Pitkänen, 1995; Sorvari, Soininen,
& Pitkänen, 1996a; Sorvari, Soininen, & Pitkänen, 1996b)—there is almost
complete homology between the two species. There is, however, virtually no
available information on the connectivity of the human amygdala. Thus find-
ings from the nonhuman primate provide the most reasonable estimate of the
neuroanatomical relationships in which the human amygdala is involved.
CytoArCHIteCtonIC orgAnIzAtIon
The amygdaloid complex is a heterogeneous group of nuclei and cortical
regions located in the medial temporal lobe just rostral to the hippocampal
formation. The nonhuman primate amygdaloid complex can be divided into
13 nuclei and cortical areas (Amaral & Bassett, 1989; Amaral et al., 1992;
Gloor, 1997; Pitkänen & Amaral, 1998; Price et al., 1987) (Figure 1.1). For
convenience, these often are classified as “deep nuclei” (the lateral nucleus
[abbreviated as L in Figure 1.1], basal nucleus [B in Figure 1.1], accessory
basal nucleus [AB], and paralaminar nucleus [PL]); “superficial nuclei” (the
medial nucleus [M], the anterior cortical nucleus [COa], the posterior cortical
nucleus [COp], the nucleus of the lateral olfactory tract [NLOT], and the peri-
amygdaloid cortex [PAC]); and “remaining nuclei” (the anterior amygdaloid
area [AAA], the central nucleus [CE], the amygdalohippocampal area [AHA],
and the intercalated nuclei [I]) (Table 1.1). We have provided a series of cor-
onal sections (Figures 1.1A–1.1G) in which the locations and rostrocaudal
extents of each of these nuclei and cortical areas are indicated. It is important
to provide this full series of sections, since some nuclei are only located at
certain rostrocaudal levels. The central nucleus, for example, is only found
within the caudal half of the amygdaloid complex. We now provide a bit more
detail on the organization and intrinsic connections of each of these regions.
The intrinsic connections are summarized in Figure 1.2.
SubDIvISIonS, CytoArCHIteCture,
AnD IntrA- AMygDAloID ConneCtIvIty
Deep Nuclei
Lateral Nucleus
The lateral nucleus is subdivided into dorsal, dorsal intermediate, ventral
intermediate, and ventral divisions (Pitkänen & Amaral, 1998; Price et al.,
1987) on the basis of cell density, size, and chemoarchitechtonics. Neurons in
the dorsal divisions are less densely packed and stain weakly for acetylcholin-
neuroanatomy of the Primate amygdala 5
FIgure 1.1.
6 FROm animal mOdels TO human amygdala FunCTiOn
FIgure 1.1.