Behavioural Brain Research 316 (2017) 261–270
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Behavioural Brain Research
jou rn al hom epage: www.elsevier.com/locate/bbr
Research report
Metabolic activation of amygdala, lateral septum and accumbens
circuits during food anticipatory behavior
Diana Olivo
a
, Mario Caba
b
, Francisco Gonzalez-Lima
c
, Juan F. Rodríguez-Landa
d
,
Aleph A. Corona-Morales
e,∗
a
Programa de Doctorado en Ciencias Biomédicas, Universidad Veracruzana, Xalapa, Veracruz 91190, Mexico
b
Centro de Investigaciones Biomédicas, Universidad Veracruzana, Xalapa, Veracruz 91190, Mexico
c
Department of Psychology and Institute for Neuroscience, The University of Texas at Austin, Austin, TX 78712, USA
d
Laboratorio de Neurofarmacología, Instituto de Neuroetología, Universidad Veracruzana, Xalapa, Veracruz 91190, Mexico
e
Laboratorio de Investigación Genómica y Fisiológica, Facultad de Nutrición, Médicos y odontólogos s/n, Col. Unidad del Bosque, 91010, Universidad
Veracruzana, Xalapa, Veracruz, Mexico
h i g h l i g h t s
•
We used cytochrome oxidase histochemistry to study brain metabolic circadian rhythms.
•
Neural rhythms were studied in rabbit pups entrained to circadian feeding.
•
Extended amygdala, lateral septum and accumbens core peaked during food anticipation.
•
Accumbens shell, caudate, putamen and cortical amygdala peaked after feeding.
•
Temporal conditioning circuits may contribute to food anticipatory activity.
a r t i c l e i n f o
Article history:
Received 9 May 2016
Received in revised form 25 August 2016
Accepted 6 September 2016
Available online 9 September 2016
Keywords:
Circadian rhythm ontogeny
Cytochrome oxidase histochemistry
Food anticipatory activity
Conditioned emotional behavior
Reward expectation
a b s t r a c t
When food is restricted to a brief fixed period every day, animals show an increase in temperature,
corticosterone concentration and locomotor activity for 2–3 h before feeding time, termed food anticipa-
tory activity. Mechanisms and neuroanatomical circuits responsible for food anticipatory activity remain
unclear, and may involve both oscillators and networks related to temporal conditioning. Rabbit pups are
nursed once-a-day so they represent a natural model of circadian food anticipatory activity. Food antici-
patory behavior in pups may be associated with neural circuits that temporally anticipate feeding, while
the nursing event may produce consummatory effects. Therefore, we used New Zealand white rabbit pups
entrained to circadian feeding to investigate the hypothesis that structures related to reward expectation
and conditioned emotional responses would show a metabolic rhythm anticipatory of the nursing event,
different from that shown by structures related to reward delivery. Quantitative cytochrome oxidase
histochemistry was used to measure regional brain metabolic activity at eight different times during
the day. We found that neural metabolism peaked before nursing, during food anticipatory behavior,
in nuclei of the extended amygdala (basolateral, medial and central nuclei, bed nucleus of the stria ter-
minalis), lateral septum and accumbens core. After pups were fed, however, maximal metabolic activity
was expressed in the accumbens shell, caudate, putamen and cortical amygdala. Neural and behavioral
activation persisted when animals were fasted by two cycles, at the time of expected nursing. These
findings suggest that metabolic activation of amygdala-septal-accumbens circuits involved in temporal
conditioning may contribute to food anticipatory activity.
© 2016 Elsevier B.V. All rights reserved.
Abbreviations: CO, cytochrome oxidase; FAA, food anticipatory activity; OD, optical density; PD, postnatal day; ROD, relative optical density; ZT, zeitgeber time.
∗
Corresponding author.
E-mail addresses: dolivormz@gmail.com (D. Olivo), mcaba@uv.mx (M. Caba), gonzalezlima@utexas.edu (F. Gonzalez-Lima), juarodriguez@uv.mx (J.F. Rodríguez-Landa),
alecorona@uv.mx, cmaa0@yahoo.com (A.A. Corona-Morales).
http://dx.doi.org/10.1016/j.bbr.2016.09.015
0166-4328/© 2016 Elsevier B.V. All rights reserved.