Payton, Colleen A.

Wesson, Daniel W.

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Colleen A. Payton

Daniel W. Wesson

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Frontiers in Neuroanatomy

Amygdaloid?Striatal Substrates Underlying Odor Hedonics and Odor-Guided Behaviors

Colleen A Payton

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Amygdaloid-striatal substrates underlying odor hedonics and odor-guided behaviors

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NEUROANATOMY
tory tubercle by the amygdala. The olfac-
tory tubercle is a striatal structure with a 
cortical-like organization which displays 
odor-evoked activity and may be criti-
cal for olfactory perception (Wesson and 
Wilson, 2011). The anatomical findings by 
Novejarque et al. (2011) along with those 
of previous groups (Usunoff et al., 2009) 
suggest the involvement of the olfactory 
tubercle (and perhaps the tubercle’s strong 
connections with the basal ganglia) in the 
emotional regulation of olfactory percep-
tion and the strong hedonic responses 
evoked by odors (e.g., Herz and Cupchick, 
1995). Despite this, without data showing 
the role of the olfactory tubercle to olfactory 
processing, little can be inferred regarding 
the amygdala innervation of the olfactory 
tubercle.
Another major contribution of the pre-
sent study was the finding that all cortical 
amygdaloid nuclei (excluding the piri-
form cortex) innervate the major island 
of Calleja. This was especially the case for 
the posteromedial cortical amygdaloid 
nucleus. The islands of Calleja are dense 
granule cell clusters residing mostly within 
layers II and III of the olfactory tubercle in 
rodents and largely in the nucleus accum-
bens in humans. However, the function of 
the islands of Calleja is unknown. Thus 
while this finding by Novejarque et al. 
(2011) is difficult to interpret in terms 
of functional consequences, it is almost 
undoubted that the amygdala’s dense 
innervation of the major island of Calleja 
will be found important to the emotional 
modulation of odor perception (given 
their positioning within the olfactory 
tubercle) and to the regulation of socio-
sexual behaviors.
There are ample future directions to link 
these anatomical findings by Novejarque 
et al. (2011) to functional significance. First, 
and most recently discussed, would elimi-
nation or inactivation of the major island of 
Calleja abolish associative changes in odor 
hedonics? This of course is based upon the 
Amygdaloid–striatal substrates underlying odor hedonics and 
odor-guided behaviors
Colleen A. Payton and Daniel W. Wesson*
Department of Neurosciences, Case Western Reserve University School of Medicine, Cleveland, OH, USA
*Correspondence: dww53@case.edu
A commentary on
Amygdaloid projections to the ventral 
striatum in mice: direct and indirect chem-
osensory inputs to the brain reward system
by Novejarque, A., Gutiérrez-Castellanos, 
N., Lanuza, L., and Martínez-García, F. 
(2011). Front. Neuroanat. 5:54. doi: 10.3389/
fnana.2011.00054
Imagine taking a long sniff of your favorite 
dinner plate, and the strong sense of pleas-
ure felt as you anticipate eating and even-
tually filing your hunger. Now, imagine the 
transient perception of sour milk from the 
carton and the rapid disgust this evoked. 
Olfactory system-mediated perception of 
odors has an astounding capacity to evoke 
emotional and behavioral responses (Kirk-
Smith et al., 1983; Herz and Cupchick, 1995). 
This phenomenon is often attributed to the 
direct connections between primary olfac-
tory structures (the main and accessory 
olfactory bulbs) and the amygdala. While 
the amygdala is indeed crucial for emotional 
responses (LeDoux, 2000), other structures, 
including those within the ventral striatum, 
likely perform similar functions in link-
ing olfactory sensory input with appro-
priate behavioral responses (Wesson and 
Wilson, 2011). Thus, an understanding of 
the  striatal–amygdala connectivity is para-
mount in elucidating the neural substrates 
for odor-evoked cognitive functions and 
behavioral responses.
Addressing this need, Novejarque et al. 
(2011) recently provided a masterfully 
detailed analysis of the amygdaloid nuclei 
projections to the ventral striato-pallidum. 
The authors employed anterograde and ret-
rograde tract-tracing experiments in mice 
to examine amygdala connectivity with the 
olfactory tubercle, the nucleus accumbens, 
and the islands of Calleja. The authors 
demonstrated “direct” projections to the 
ventral striato-pallidum from the chem-
osensory cortical amygdala and “indirect” 
projections from the associative amygdala 
nuclei. Novejarque et al. (2011) hypothesize 
that the direct projections may be stimu-
lated through an unconditioned response 
to odors, possibly pheromones, whereas the 
indirect projections would likely be stimu-
lated through a learned response to associ-
ated stimuli. These projections interconnect 
with the nucleus accumbens, olfactory 
tubercle, and islands of Calleja in a man-
ner possibly important for olfactory per-
ception and odor-guided behaviors. Several 
notable findings stand out as promising in 
understanding the neuroanatomical basis 
for odor hedonics.
While amygdala innervation of the 
nucleus accumbens’ core and shell regions 
has received considerable attention (e.g., 
Everitt et al., 1999), none were performed 
with such detail in mice as that performed by 
Novejarque et al. (2011). The  amygdaloid–
striatal projections likely subserve the 
expression of reward-related behaviors 
toward secondary reinforcers (Cador et al., 
1989). In addition, these indirect projec-
tions may underlie learning-related modu-
lation of odor hedonics as Novejarque et al. 
(2011) hypothesize. Thus, this information 
pathway is likely critical to the majority of 
our odor-based olfactory decisions and 
behaviors, which are arguably based upon 
learning more-so than innate preferences, 
or aversions. Perhaps correlating with the 
complexity and diversity of these learned 
behaviors, the authors report that the fiber 
pathways between the amygdala and ven-
tral striatum (the stria terminalis, ansa 
peduncularis, and longitudinal association 
bundle) vary in density and destination 
depending upon their origin. These fiber 
pathways are likely to promote the regula-
tion of social and sexual behaviors through 
hedonic functions as has been suggested 
from work in humans (Fox et al., 2010; 
Somerville et al., 2011).
Similar to that reported over previous 
years (Fallon et al., 1983; Ubeda-Bañona 
et al., 2007; Usunoff et al., 2009), the authors 
observed the dense innervation of the olfac-
Frontiers in Neuroanatomy www.frontiersin.org September 2011 | Volume 5 | Article 61 | 1
General Commentary
published: 26 September 2011
doi: 10.3389/fnana.2011.00061
Marcos, A. (2007). Projections from the posterolat-
eral olfactory amygdala to the ventral striatum: neural 
basis for reinforcing  properties of chemical stimuli. 
BMC Neurosci. 8, 103. doi: 10.1186/1471-2202-8-103
Usunoff, K. G., Schmitt, O., Itzev, D. E., Haas, S. J. P., 
Lazarov, N. E., Rolfs, A., and Wree, A. (2009). Efferent 
projections of the anterior and posterodorsal regions 
of the medial nucleus of the amygdala in the mouse. 
Cells Tissues Organs 190, 256–285.
Wesson, D. W., and Wilson, D. A. (2011). Sniffing out the 
contributions of the olfactory tubercle to the sense 
of smell: hedonics, sensory integration, and more? 
Neurosci. Biobehav. Rev. 35, 655–668.
Zahm, D. S., and Heimer, L. (1993). Specificity in the 
efferent projections of the nucleus accumbens in the 
rat: comparison of the rostral pole projection patterns 
with those of the core and shell. J. Comp. Neurol. 327, 
220–232.
Received: 15 August 2011; accepted: 07 September 2011; 
published online: 26 September 2011.
Citation: Payton CA and Wesson DW (2011) Amygdaloid–
striatal substrates underlying odor hedonics and odor-
guided behaviors. Front. Neuroanat. 5:61. doi: 10.3389/
fnana.2011.00061
Copyright © 2011 Payton and Wesson. This is an open-
access article subject to a non-exclusive license between 
the authors and Frontiers Media SA, which permits use, 
distribution and reproduction in other forums, provided 
the original authors and source are credited and other 
Frontiers conditions are complied with.
dala-ventral striatal subsystems. Ann. N. Y. Acad. Sci. 
877, 412–438.
Fallon, J. H., Loughlin, S. E., and Ribak, C. E. (1983). The 
islands of Calleja complex of rat basal forebrain. III. 
Histochemical evidence for a striatopallidal system. 
J. Comp. Neurol. 218, 91–120.
Fox, A. S., Shelton, S. E., Oakes, T. R., Converse, A. K., 
Davidson, R. J., and Kalin, N. H. (2010). Orbitofrontal 
cortex lesions alter anxiety-related activity in the pri-
mate bed nucleus of stria terminalis. J. Neurosci. 30, 
7023–7027.
Herz, R. S., and Cupchick, G. C. (1995). The emotional 
distinctiveness of odor-evoked memories. Chem. 
Senses 20, 517–528.
Kirk-Smith, M. D., van Toller, C., and Dodd, G. H. (1983). 
Unconscious odour conditioning in human subjects. 
Biol. Psychol. 17, 221–231.
LeDoux, J. E. (2000). Emotion circuits in the brain. Annu. 
Rev. Neurosci. 23, 155–184.
Novejarque, A., Gutierrez-Castellanos, N., Lanuza, E., and 
Martinez-Garcia, F. (2011). Amygdaloid projections 
to the ventral striatum in mice: direct and indirect 
chemosensory inputs to the brain reward system. 
Front. Neuroanat. 5:54. doi: 10.3389/fnana.2011.00054
Somerville, L. H., Whalen, P. J., and Kelley, W. M. (2011). 
Human bed nucleus of the stria terminalis indexes 
hypervigilant threat monitoring. Biol. Psychiatry 68, 
416–424.
Ubeda-Bañona, I., Novejarque, A., Mohedano-Moriano, 
A., Pro-Sistiaga, P., de la Rosa-Prieto, C., Insausti, 
R., Martinez-Garcia, F., Lanuza, E., and Martinez-
assumption that the islands of Calleja do 
in fact play a role in odor processing and/
or reward processes. Related, are particular 
amygdala outputs to these structures (the 
nucleus accumbens, olfactory tubercle, or 
islands of Calleja) more strongly involved 
in relaying hedonic information? Finally, 
given the known interconnections between 
the olfactory tubercle and nucleus accum-
bens (Zahm and Heimer, 1993), are the dis-
tinct inputs to each of these structures from 
the amygdala simply redundant, or do they 
each provide unique information regarding 
emotionally relevant processes? Answers to 
these and other questions will help us along 
our way to understanding the neural basis 
of odor hedonics and ultimately behaviors 
driven in large part by odor hedonics.
RefeRences
Cador, M., Robbins, T. W., and Everitt, B. J. (1989). 
Involvement of the amygdala in stimulus-reward 
associations: interaction with the ventral striatum. 
Neuroscience 30, 77–86.
Everitt, B. J., Parkinson, J. A., Olmstead, M. C., Arroyo, 
M., Robledo, P., and Robbins, T. W. (1999). Associative 
processes in addiction and reward. The role of amyg-
Payton and Wesson Anatomical substrates of odor hedonics
Frontiers in Neuroanatomy www.frontiersin.org September 2011 | Volume 5 | Article 61 | 2


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Amygdaloid–Striatal Substrates Underlying Odor Hedonics and Odor-Guided Behaviors

Amygdaloid–Striatal Substrates Underlying Odor Hedonics and Odor-Guided Behaviors

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