Functional magnetic resonance imaging shows oxytocin activates brain regions associated with mother-pup bonding during suckling

Journal of Neuroscience

Volumn 25, Issue 50, 2005, Pages 11637-11644

  Febo, Marcelo ^a   Numan, Michael ^b   Ferris, Craig F ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b BOSTON COLLEGE   (United States)

Author keywords

Imaging; Lactation; Maternal; Olfactory; Oxytocin; Somatosensory

Indexed keywords

OXYTOCIN; OXYTOCIN RECEPTOR; OXYTOCIN RECEPTOR ANTAGONIST; RECEPTOR BLOCKING AGENT; UNCLASSIFIED DRUG;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ARTICLE; BRAIN REGION; BREAST FEEDING; CONTROLLED STUDY; EMOTIONAL ATTACHMENT; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HYPOTHALAMUS; INSULA; NONHUMAN; NUCLEUS ACCUMBENS; OLFACTORY SYSTEM; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; SUCKLING; VENTRAL TEGMENTUM;

ANIMALS; ANIMALS, SUCKLING; BRAIN MAPPING; EMOTIONS; FEMALE; MAGNETIC RESONANCE IMAGING; MATERNAL BEHAVIOR; OBJECT ATTACHMENT; OXYTOCIN; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, OXYTOCIN; REWARD;

EID: 30744464849     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3604-05.2005     Document Type: Article

References (49)

1. Byrnes EM, Rigero BA, Bridges RS (2002) Dopamine antagonists during parturition disrupt maternal care and the retention of maternal behavior in rats. Pharmacol Biochem Behav 73:869-875.
2. Champagne F, Diorio J, Sharma S, Meaney MJ (2001) Naturally occurring variations in maternal behavior in the rat are associated with differences in estrogen-inducible central oxytocin receptors. Proc Natl Acad Sci USA 98:12736-12741.
3. Febo M, Segarra AC, Tenney JR, Brevard ME, Duong TQ, Ferris CF (2004) Imaging cocaine-induced changes in the mesocorticolimbic dopaminergic system of conscious rats. J Neurosci Methods 139:167-176.
4. Ferris CF, Kulkarni P, Sullivan Jr JM, Harder JA, Messenger TL, Febo M (2005) Pup suckling is more rewarding than cocaine: evidence from functional magnetic resonance imaging and three-dimensional computational analysis. J Neurosci 25:149-156.
5. Fleming A, Vaccarino F, Tambosso L, Chee P (1979) Vomeronasal and olfactory system modulation of maternal behavior in the rat. Science 203:372-374.
6. Francis DD, Champagne FC, Meaney MJ (2000) Variations in maternal behaviour are associated with differences in oxytocin receptor levels in the rat. J Neuroendocrinol 12:1145-1148.
7. Genovese CR, Lazar NA, Nichols T (2002) Thresholding of statistical maps in functional neuroimaging using the false discovery rate. NeuroImage 15:870-878.
8. Hansen S, Bergvall AH, Nyiredi S (1993) Interaction with pups enhances dopamine release in the ventral striatum of maternal rats: a microdialysis study. Pharmacol Biochem Behav 45:673-676.
9. Insel TR, Harbaugh CR (1989) Lesions of the hypothalamic paraventricular nucleus disrupt the initiation of maternal behavior. Physiol Behav 45:1033-1041.
10. Kendrick KM, Da Costa AP, Broad KD, Ohkura S, Guevara R, Levy F, Keverne EB (1997) Neural control of maternal behaviour and olfactory recognition of offspring. Brain Res Bull 44:383-395.
11. King JA, Garelick TS, Brevard ME, Chen W, Messenger TL, Duong TQ, Ferris CF (2005) Procedure for minimizing stress for fMRI studies in conscious rats. J Neurosci Methods 148:154-160.
12. Lancel M, Krömer S, Neumann ID (2003) Intracerebral oxytocin modulates sleep-wake behaviour in male rats. Regul Pept 114:145-152.
13. Lee A, Li M, Watchus J, Fleming AS (1999) Neuroanatomical basis of maternal memory in postpartum rats: selective role for the nucleus accumbens. Behav Neurosci 113:523-538.
14. Levy F, Kendrick KM, Keverne EB, Piketty V, Poindron P (1992) Intracerebral oxytocin is important for the onset of maternal behavior in inexperienced ewes delivered under peridural anesthesia. Behav Neurosci 106:427-432.
15. Li C, Chen P, Smith MS (1999) Neural populations of the rat forebrain and brainstem activated by the suckling stimulus as demonstrated by cFos expression. Neuroscience 94:117-129.
16. Li M, Fleming AS (2003) The nucleus accumbens shell is critical for normal expression of pup-retrieval in postpartum female rats. Behav Brain Res 145:99-111.
17. Lin SH, Miyata S, Matsunaga W, Kawarabayashi T, Nakashima T, Kiyohara T (1998) Metabolic mapping of the brain in pregnant, parturient and lactating rats using Fos immunohistochemistry. Brain Res 787:226-236.
18. Lonstein JS, Stern JM (1997) Role of the midbrain periaqueductal gray in maternal nurturance and aggression: c-fos and electrolytic lesion studies in lactating rats. J Neurosci 17:3364-3378.
19. Lonstein JS, Simmons DA, Swann JM, Stern JM (1998) Forebrain expression of c-fos due to active maternal behaviour in lactating rats. Neuroscience 82:267-281.
20. Ludwig R, Bodgdanov G, King J, Allard A, Ferris CF (2004) A dual RF resonator system for high-field functional magnetic resonance imaging of small animals. J Neurosci Methods 132:125-135.
21. Mattson BJ, Williams S, Rosenblatt JS, Morrell JI (2001) Comparison of two positive reinforcing stimuli: pups and cocaine throughout the postpartum period. Behav Neurosci 115:683-694.
22. Neumann I, Russell JA, Landgraf R (1993a) Oxytocin and vasopressin release within the supraoptic and paraventricular nuclei of pregnant, parturient and lactating rats: a microdialysis study. Neuroscience 53:65-75.
23. Neumann I, Ludwig M, Engelmann M, Pittman QJ, Landgraf R (1993b) Simultaneous microdialysis in blood and brain: oxytocin and vasopressin release in response to central and peripheral osmotic stimulation and suckling in the rat. Neuroendocrinology 58:637-645.
24. Neumann I, Koehler E, Landgraf R, Summy-Long J (1994) An oxytocin receptor antagonist infused into the supraoptic nucleus attenuates intranuclear and peripheral release of oxytocin during suckling in conscious rats. Endocrinology 134:141-148.
25. NumanM (1994) A neural circuitry analysis of maternal behavior in the rat. Acta Paediatr Suppl 397:19-28.
26. Numan M (2004) Maternal behaviors: central integration or independent parallel circuits? Theoretical comments on Popeski and Woodside. Behav Neurosci 118:1469-1472.
27. Numan M, Corodimas KP (1985) The effects of paraventricular hypothalamic lesions on maternal behavior in rats. Physiol Behav 35:417-425.
28. Numan M, Numan MJ (1996) A lesion and neuroanatomical tract-tracing analysis of the role of the bed nucleus of the stria terminalis in retrieval behavior and other aspects of maternal responsiveness in rats. Dev Psychobiol 29:23-51.
29. Numan M, Smith HG (1984) Maternal behavior in rats: evidence for the involvement of preoptic projections to the ventral tegmental area. Behav Neurosci 98:712-727.
30. Numan M, Numan MJ, Schwarz JM, Neuner CM, Flood TF, Smith CD (2005) Medial preoptic area interactions with the nucleus accumbensventral pallidum circuit and maternal behavior in rats. Behav Brain Res 158:53-68.
31. Numan MJ, Insel TR (2003) The neurobiology of parental behavior, Ed 3. New York: Springer.
32. Paxinos G, Watson C (1997) The rat brain in stereotaxic coordinates, Vol 1, Ed 3. Boston: Academic.
33. Pedersen CA, Boccia ML (2003) Oxytocin antagonism alters rat dams' oral grooming and upright posturing over pups. Physiol Behav 80:233-241.
34. Pedersen CA, Prange Jr AJ (1979) Induction of maternal behavior in virgin rats after intracerebroventricular administration of oxytocin. Proc Natl Acad Sci USA 76:6661-6665.
35. Pedersen CA, Caldwell JD, Walker C, Ayers G, Mason GA (1994) Oxytocin activates the postpartum onset of rat maternal behavior in the ventral tegmental and medial preoptic areas. Behav Neurosci 108:1163-1171.
36. Pedersen CA, Johns JM, Musiol I, Perez-Delgado M, Ayers G, Faggin B, Caldwell JD (1995) Interfering with somatosensory stimulation from pups sensitizes experienced, postpartum rat mothers to oxytocin antagonist inhibition of maternal behavior. Behav Neurosci 109:980-990.
37. Price JL (1973) An autoradiographic study of complementary laminar patterns of termination of afferent fibers to the olfactory cortex. J Comp Neurol 150:87-108.
38. Simerly RB, Swanson LW (1988) Projections of the medial preoptic nucleus: a Phaseolus vulgaris leucoagglutinin anterograde tract-tracing in the rat. J Comp Neurol 270:209-242.
39. Slotnick BM, Nigrosh BJ (1975) Maternal behavior of mice with cingulate cortical, amygdala, or septal lesions. J Comp Physiol Psychol 88:118-127.
40. Stack EC, Balakrishnan R, Numan MJ, NumanM (2002) A functional neuroanatomical investigation of the role of the medial preoptic area in neural circuits regulating maternal behavior. Behav Brain Res 131:17-36.
41. Strupp JP (1996) Stimulate: a GUI based fMRI analysis software package. NeuroImage 3:S607.
42. Swanson LW (1999) Brain maps: structure of the rat brain, Ed 2. Boston: Elsevier Science.
43. Tribollet E, Barberis C, Dreifuss JJ, Jard S (1988) Autoradiographic localization of vasopressin and oxytocin binding sites in rat kidney. Kidney Int 33:959-965.
44. Vaccari C, Lolait SJ, Ostrowski NL (1998) Comparative distribution of vasopressin V1b and oxytocin receptor messenger ribonucleic acids in brain. Endocrinology 139:5015-5033.
45. van Leengoed E, Kerker E, Swanson HH (1987) Inhibition of post-partum maternal behaviour in the rat by injecting an oxytocin antagonist into the cerebral ventricles. J Endocrinol 112:275-282.
46. Veinante P, Freund-Mercier MJ (1997) Distribution of oxytocin- and vasopressin-binding sites in the rat extended amygdala: a histoautoradiographic study. J Comp Neurol 383:305-325.
47. Witt DM, Insel TR (1991) A selective oxytocin antagonist attenuates progesterone facilitation of female sexual behavior. Endocrinology 128:3269-3276.
48. Wu Z, Sullivan JMJ (2003) Multiple material marching cubes algorithm. IJNME 58:189-207.
49. Yoshimura R, Kiyama H, Kimura T, Araki T, Maeno H, Tanizawa O, Tohyama M (1993) Localization of oxytocin receptor messenger ribonucleic acid in the rat brain. Endocrinology 133:1239-1246.