Differential changes of metabolic brain activity and interregional functional coupling in prefronto-limbic pathways during different stress conditions: Functional imaging in freely behaving rodent pups

Frontiers in Cellular Neuroscience

Volumn , Issue MAY 2012, 2012, Pages

  Bock, Jörg ^a,b   Riedel, Anett ^b   Braun, Katharina ^a,b  

^a Center for Behavioral Brain Sciences   (Germany)

^b OTTO VON GUERICKE UNIVERSITY   (Germany)

Author keywords

Functional coupling; Functional imaging; Limbic system; Maternal separation; PAG; Prefrontal cortex; Stress

Indexed keywords

FLUORODEOXYGLUCOSE F 18;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIORAL STRESS; BRAIN FUNCTION; CONTROLLED STUDY; CORPUS CALLOSUM; CORPUS STRIATUM; DOWN REGULATION; ELECTROENCEPHALOGRAPHY; EMOTIONALITY; FUNCTIONAL ASSESSMENT; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HABENULA; HIPPOCAMPUS; LIMBIC SYSTEM; MALE; MATERNAL DEPRIVATION; NEUROIMAGING; NONHUMAN; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX;

EID: 84864018999     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2012.00019     Document Type: Article

References (69)

1. Bassett, D. S., and Bullmore, E. T. (2009). Human brain networks in health and disease. Curr. Opin. Neurol. 22, 340-347.
2. Bock, J., and Braun, K. (2011). The impact of perinatal stress on the functional maturation of prefronto-cortical synaptic circuits: implications for the pathophysiology of ADHD? Prog. Brain Res. 189, 155-169.
3. Bock, J., Schnabel, R., and Braun, K. (1997). Role of the dorso-caudal neostriatum in filial imprinting of the domestic chick: a pharmacological and autora-diographical approach focused on the involvement of NMDA-receptors. Eur. J. Neurosci. 9, 1262-1272.
4. Bock, J., Wolf, A., and Braun, K. (1996). Influence of the N-methyl-D-aspartate receptor antagonist DL-2-amino-5-phosphonovaleric acid on auditory filial imprinting in the domestic chick. Neurobiol. Learn. Mem. 65, 177-188.
5. Brandão, M. L., Zanoveli, J. M., Ruiz-Martinez, R. C., Oliveira, L. C., and Landeira-Fernandez, J. (2008). Different patterns of freezing behavior organized in the periaqueductal gray of rats: association with different types of anxiety. Behav. Brain Res. 188, 1-13.
6. Braun, K., and Bock, J. (2011). The experience-dependent maturation of prefronto-limbic circuits and the origin of developmental psychopathology: implications for the pathogenesis and therapy of behavioural disorders. Dev. Med. ChildNeurol. 53, 14-18.
7. Braun, K., Kremz, P., Wetzel, W., Wagner, T., and Poeggel, G. (2003). Influence of parental deprivation on the behavioural development in Octodon degus: modulation by maternal vocalizations. Dev. Psychobiol. 42, 237-245.
8. Braun, K., and Poeggel, G. (2001). Recognition of mother's voice evokes metabolic activation in the medial prefrontal cortex and lateral thalamus of Octodon degus pups. Neuroscience 103, 861-864.
9. Braun, S., and Scheich, H. (1997). Influence of experience on the representation of the "mothering call" in frontoparietal and auditory cortex of pups of the rodent Octodon degus: FDG mapping. J. Comp. Physiol. A 181, 697-709.
10. Chih, C. P., Lipton, P., and Roberts, E. L. Jr. (2001). Do active cerebral neurons really use lactate rather than glucose? Trends Neurosci. 24, 573-578.
11. Colonnello, V., Iacobucci, P., Fuchs, T., Newberry, R. C., and Panksepp, J. (2011). Octodon degus. A useful animal model for social-affective neuroscience research: basic description of separation distress, social attachments and play. Neurosci. Biobehav. Rev. 35, 1854-1863.
12. Damasio, A. R., Grabowski, T. J., Bechara, A., Damasio, H., Ponto, L. L., Parvizi, J., and Hichwa, R.D. (2000). Subcortical and cortical brain activity during the feeling of self-generated emotions. Nat. Neurosci. 3, 1049-1056.
13. Del Casale, A., Kotzalidis, G. D., Rapinesi, C., Serata, D., Ambrosi, E., Simonetti, A., Pompili, M., Ferracuti, S., Tatarelli, R., and Girardi P. (2011). Functional neuroimaging in obsessive-compulsive disorder. Neuropsychobiology 64, 61-85.
14. Duncan, G. E., Johnson, K. B., and Breese, G. R. (1993). Topographic patterns ofbrain activityinresponse to swim stress: assessment by 2-deoxyglucose uptake and expression of Fos-like immunoreactivity. J. Neurosci. 13, 3932-3943.
15. Fuchs, E., Flugge, G., and Czeh, B. (2006). Remodeling of neuronal networks by stress. Front. Biosci. 11, 2746-2758.
16. Fuchs, T., Lacobucci, P., MacKinnon, K. M., and Panksepp, J. (2010). Infant-mother recognition in a social rodent (Octodon degus). J. Comp. Psychol. 124, 166-175.
17. Gonzalez-Lima, F. (1992). "Brain imaging of auditory learning functions in rats: studies with flu-orodeoxyglucose autoradiography and cytochrome oxidase histochemistry", in Advances in Metabolic Mapping Techniques for Brain Imaging of Behavioral and Learning Functions, eds F. Gonzalez-Lima, F. T. Finkenstädt, and H. Scheich (Kluwer Academic Publishers), 39-109.
18. Gonzalez-Lima, F., and Scheich, H. (1986). Neural substrates for tone-conditioned bradycardia demonstrated with 2-deoxyglucose. II. Auditory cortex plasticity. Behav. Brain Res. 20, 281-293.
19. Graeff, F. G. (2004). Serotonin, the periaqueductal gray and panic. Neurosci. Biobehav. Rev. 28, 239-259.
20. Gruss, M., Westphal, S., Luley, C., and Braun, K. (2006). Endocrine and behavioural plasticity in response to juvenile stress in the semi-precocial rodent Octodon degus. Psychoneuroendocrinology 31, 361-372.
21. Guterman, A., and Richter-Levin, G. (2006). Neuromodulators of LTP and NCAMs in the amygdala and hippocampus in response to stress. EXS98, 137-148.
22. Heim, C., and Nemeroff, C. B. (2001). The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies. Biol. Psychiatry 49, 1023-1039.
23. Heim, C., Shugart, M., Craighead, W. E., and Nemeroff, C. B. (2010). Neurobiological and psychiatric consequences of child abuse and neglect. Dev. Psychobiol. 52, 671-690.
24. Henckens, J. A. G., van Wingen, G. A., Joels, M., and Fernandez, G. (2011). Corticosteroid induced decoupling of the amygdala in men. Cereb. Cortex. [Epub ahead of print].
25. Horner, H. C., Packan, D. R., and Sapolsky, R. M. (1990). Glucocorticoids inhibit glucose transport in cultured hippocampal neurons and glia. Neuroendocrinology 52, 57-64.
26. Hulvershorn, L. A., Cullen, K., and Anand, A. (2011). Toward dysfunctional connectivity: a review of neuroimaging findings in pediatric major depressive disorder. Brain ImagingBehav. 5, 307-328.
27. Korosi, A., and Baram, T. Z. (2009). The pathways from mother's love to baby's future. Front. Behav. Neurosci. 3:27. doi: 10.3389/neuro.08.027.2009
28. La Bar, K. S., Gatenby, J. C., Gore, J. C., LeDoux, J. E., and Phelps, E. A. (1998). Human amygdala activation during conditioned fear acquisition and extinction: a mixed-trial fMRI study. Neuron 20, 937-945.
29. Linnman, C., Moulton, E. A., Barmettler, G., Becerra, L., and Borsook, D. (2012). Neuroimaging of the periaqueductal gray: state of the field. Neuroimage 60, 505-522.
30. Liston, C., Cohen, M. M., Teslovich, T., Levenson, D., and Casey, B. J. (2011). Atypical prefrontal connectivity in attention-deficit/hyperactivity disorder: pathway to disease or pathological end point? Biol. Psychiatry 69, 1168-1177.
31. Loman, M. M., and Gunnar, M. R. (2010). Early experience and the development of stress reactivity and regulation in children. Neurosci. Biobehav. Rev. 34, 867-876.
32. Magistretti, P. J. (2006). Neuron-glia metabolic coupling and plasticity. J. Exp. Biol. 209, 2304-2311.
33. McEwen, B. S. (2010). Stress, sex, and neural adaptation to a changing environment: mechanisms of neuronal remodeling. Ann. N.Y. Acad. Sci. 1204 (Suppl.), E38-E59.
34. McIntosh, A. R., and Gonzalez-Lima, F. (1998). Large-scale functional connectivity in associative learning: interrelations of the rat auditory, visual, and limbic systems. J. Neurophysiol. 80, 3148-3162.
35. Minshew, N. J., and Keller, T. A. (2010). The nature of brain dysfunction in autism: functional brain imaging studies. Curr. Opin. Neurol. 23, 124-130.
36. Mobbs, D., Marchant, J. L., Hassabis, D., Seymour, B., Tan, G., Gray, M., Petrovic, P., Dolan, R. J., and Frith, C. D. (2009). From threat to fear: the neural organization of defensive fear systems in humans. J. Neurosci. 29, 12236-12243.
37. Moriceau, S., and Sullivan, R. M. (2006). Maternal presence serves as a switch between learning fear and attraction in infancy. Nat. Neurosci. 9, 1004-1006.
38. Munck, A. (1971). Glucocorticoid inhibition of glucose uptake by peripheral tissues: old and new evidence, molecular mechanisms, and physiological significance. Perspect. Biol. Med. 14, 265-269.
39. Nair, H. P., Berndt, J. D., Barrett, D., and Gonzalez-Lima, F. (2001). Maturation of extinction behavior in infant rats: large-scale regional interactions with medial pre-frontal cortex, orbitofrontal cortex, and anterior cingulate cortex. J. Neurosci. 21, 4400-4407.
40. Nair, H. P., and Gonzalez-Lima, F. (1999). Extinction of behavior in infant rats: development of functional coupling between septal, hippocampal, and ventral tegmental regions. J. Neurosci. 19, 8646-8655.
41. Neumann, I. D., Wegener, G., Homberg, J. R., Cohen, H., Slattery, D. A., Zohar, J., Olivier, J. D., and Mathé, A. A. (2010). Animal models of depression and anxiety: what do they tell us about human condition? Prog. Neuropsychopharmacol. Biol. Psychiatry35, 1357-1375.
42. Panksepp, J. (2003). At the interface of the affective, behavioral, and cognitive neurosciences: decoding the emotional feelings of the brain. Brain Cogn. 52, 4-14.
43. Panksepp, J. (2011). The basic emotional circuits of mammalian brains: do animals have affective lives? Neurosci. Biobehav. Rev. 35, 1791-1804.
44. Paxinos, G., and Watson, W. (1998). The Rat Brain in Stereotaxic Coordinates, 4th Edn. San Diego, CA: Academic Press.
45. Pechtel, P., and Pizzagalli, D. A. (2010). Effects of early life stress on cognitive and affective function: an integrated review of human literature. Psychopharmacology (Berl.) 214, 55-70.
46. Pessoa, L. (2008). On the relationship between emotion and cognition. Nat. Rev. Neurosci. 9, 148-158.
47. Phelps, E. A., O'Connor, K. J., Gatenby, J. C., Gore, J. C., Grillon, C., and Davis, M. (1998). Activation of the human amygdala by a cognitive representation of fear. Neuroimage S8, 9.
48. Poeggel, G., and Braun, K. (1997). Early auditory filial learning in degus (Octodon degus): behavioral and autoradiographic studies. Brain Res. 743, 162-170.
49. Pruessner, J. C., Dedovic, K., Khalili-Mahani, N., Engert, V., Pruessner, M., Buss, C., Renwick, R., Dagher, A., Meaney, M. J., and Lupien, S. (2008). Deactivation of the limbic system during acute psychosocial stress: evidence from positron emission tomography and functional magnetic resonance imaging studies. Biol. Psychiatry 63, 234-240.
50. Pryce, C. R., Aubert, Y., Maier, C., Pearce, P. C., and Fuchs, E. (2011). The developmental impact of prenatal stress, prenatal dexamethasone and postnatal social stress on physiology, behaviour and neuroanatomy of primate offspring: studies in rhesus macaque and common marmoset. Psychopharmacology (Berl.) 214, 33-53.
51. Riedel, A., Gruss, M., Bock, J., and Braun, K. (2010). Impaired active avoidance learning in infant rats appears to be related to insufficient metabolic recruitment of the lateral septum. Neurobiol. Learn. Mem. 93, 275-282.
52. Rilling, J. K., Winslow, J. T., O'Brien, D., Gutman, D. A., Hoffman, J. M., and Kilts, C. D. (2001). Neural correlates of maternal separation in rhesus monkeys. Biol. Psychiatry 49, 146-157.
53. Rodrigues, S. M., LeDoux, K. L., and Sapolsky, R. M. (2009). The influence of stress hormones on fear circuitry. Annu. Rev. Neurosci. 32, 289-313.
54. Sanchez, M. M., Ladd, C. O., and Plotsky, P. M. (2001). Early adverse experience as a developmental risk factor for later psychopathology: evidence from rodent and primate models. Dev. Psychopathol. 13, 419-450.
55. Sandi, C. (2004). Stress, cognitive impairment and cell adhesion molecules. Nat. Rev. Neurosci. 5, 917-930.
56. Schmidt, M. V., Wang, X. D., and Meijer, O. C. (2011). Earlylife stress paradigms in rodents: potential animal models of depression? Psychopharmacology (Berl.) 214, 131-140.
57. Sokoloff, L., Reivich, M., Kennedy, C., Des Rosiers, M. H., Patlak, C. S., Pettigrew, K. D., Sakurada, O., and Shinohara, M. (1977). The [14C]deoxyglucose method for the measurement of local cerebral glucose utilization: theory, procedure, and normal values in the conscious and anesthetized albino rat. J. Neurochem. 28, 897-916.
58. Spivey, J. M., Padilla, E., Shumake, J. D., and Gonzalez-Lima, F. (2011). Effects of maternal separation, early handling, and gonadal sex on regional metabolic capacity of the preweanling rat brain. Brain Res. 1367, 198-206.
59. Stam, C. J., and van Straaten, E. C. (2012). The organization of physiological brain networks. Clin. Neurophysiol. Feb 20. [Epub ahead of print].
60. Stevens, H. E., Leckman, J. F., Coplan, J. D., and Suomi, S. J. (2009). Risk and resilience: early manipulation of macaque social experience and persistent behavioral and neu-rophysiological outcomes. J. Am. Acad. Child Adolesc. Psychiatry 48, 114-127.
61. Uhlhaas, P. J., Roux, F., Rodriguez, E., Rotarska-Jagiela, A., and Singer, W. (2009). Neural synchrony and the development of cortical networks. Trends Cogn. Sci. 14, 72-80.
62. Virgin, C. E. Jr., Ha, T. P., Packan, D. R., Tombaugh, G. C., Yang, S. H., Horner, H. C., and Sapolsky, R. M. (1991). Glucocorticoids inhibit glucose transport and glutamate uptake in hippocampal astrocytes: implications for glucocorticoid neurotoxicity. J. Neurochem. 57, 1422-1428.
63. Wallhäusser, E., and Scheich, H. (1987). Auditory imprinting leads to differential 2-deoxyglucose uptake and dendritic spine loss in the chick rostral forebrain. Brain Res. 428, 29-44.
64. Warnock, G. I., and Steckler, T. (2011). Stress-induced decreases in local cerebral glucose utilization in specific regions of the mouse brain. BMC Res. Notes 4, 96.
65. Wiedenmayer, C. P. (2009). Plasticityof defensive behavior and fear in early development. Neurosci. Biobehav. Rev. 33, 432-441.
66. Wright, J. S., and Panksepp, J. (2011). Toward affective circuit-based pre-clinical models of depression: sensitizing dorsal PAG arousal leads to sustained suppression of positive affect in rats. Neurosci. Biobehav. Rev. 35, 1902-1915.
67. Ziabreva, I., Poeggel, G., Schnabel, R., and Braun, K. (2003a). Separation-induced receptor changes in the hippocampus and amygdala of Octodon degus: influence of maternal vocalizations. J. Neurosci. 23, 5329-5336.
68. Ziabreva, I., Schnabel, R., and Braun, K. (2000). Parental deprivation induces N-methyl-D-aspartate-receptor upregulation in limbic brain areas of Octodon degus: protective role of the maternal call. Neural. Plast. 7, 233-244.
69. Ziabreva, I., Schnabel, R., Poeggel, G., and Braun, K. (2003b). Mother's voice "buffers" separation-induced receptor changes in the pre-frontal cortex of octodon degus. Neuroscience 119, 433-441.