Temporal Memory Dysfunction and Alterations in Tyrosine Hydroxylase Immunoreactivity in Adult Rats Following Neonatal Exposure to Domoic Acid

Mark A. Robbins, Catherine L. Ryan, Amber L. Marriott, Tracy Ann Doucette

Departments of Biology University of Prince Edward, Charlottetown, Canada.
Departments of Psychology, University of Prince Edward, Charlottetown, Canada.

DOI: 10.4236/nm.2013.41005                

Abstract

The purpose of the present study was to determine whether early alterations in glutamate signaling, via daily injections of the glutamate agonist, domoic acid (DOM; 20 μg/kg), during a critical period of CNS development (PND 8 - 14), would result in temporal memory deficits and/or alterations in tyrosine hydroxylase (TH) immunoreactivity. As adults, subjects were assessed for temporal memory ability using a recency discrimination paradigm. Both number and duration of exploratory contacts directed at familiar objects, differing by one hour in recall delay, were measured. Analyses revealed that DOM-treated females demonstrated temporal memory dysfunction, as evidenced in a significantly lower proportion of total exploratory behaviour directed toward the remote object. Integrity of the dopamine system was assessed using immunohistochemistry to examine TH immunoreactivity in the prefrontal cortex (PFC) and nucleus accumbens (NAcc). Sections obtained from DOM-treated males had significantly less TH immunoreactivity in the right mPFC, while DOM-treated females had significantly greater TH immunoreactivity in the left core and right shell of the NAcc. These findings are discussed in context of early alterations to glutamate signaling in the development of human neuropsychiatric disorders.

Keywords

Domoic Acid; Glutamate; Schizophrenia; Animal Models; Neurodevelopmental Disorders

Conflicts of Interest

The authors declare no conflicts of interest.

References

[1]	S. Ozawa, H. Kamiya and K. Tsuzuki K, “Glutamate Receptors in the Mammalian Central Nervous System,” Progress in Neurobiology, Vol. 54, No. 5, 1998, pp. 581-618. doi:10.1016/S0301-0082(97)00085-3
[2]	B. Bettler and C. Mulle, “Review: Neurotransmitter Receptors II: AMPA and Kainate Receptors,” Neuropharmacology, Vol. 34, No. 2, 1995, pp. 123-139. doi:10.1016/0028-3908(94)00141-E
[3]	M. Jorgensen, C. K. Tygesen and P. H. Andersen, “Ionotropic Glutamate Receptors-Focus on Non-NMDA Receptors,” Pharmacology & Toxicology, Vol. 76, No. 5, 1995, pp. 312-319. doi:10.1111/j.1600-0773.1995.tb00153.x
[4]	D. Bleakman and D. Lodge, “Neuropharmacology of AMPA and Kainate Receptors,” Neuropharmacology, Vol. 37, No. 10-11, 1998, pp. 1187-1204. doi:10.1016/S0028-3908(98)00139-7
[5]	J. W. McDonald and M. V. Johnston, “Physiological and Pathophysiological Roles of Excitatory Amino Acids during Central Nervous System Development,” Brain Research, Brain Research Reviews, Vol. 15, No. 1, 1990, pp. 41-70. doi:10.1016/0165-0173(90)90011-C
[6]	C. G. Parsons, W. Danysz and G. Quack G, “Glutamate in CNS Disorders as a Target for Drug Development: An Update,” Drug News & Perspectivew, Vol. 11, No. 9, 1998, pp. 523-569. doi:10.1358/dnp.1998.11.9.863689
[7]	S. I. Deutsch, R. B. Rosse, B. L. Schwartz and J. Mastropaolo, “A Revised Excitotoxic Hypothesis of Schizophrenia: Therapeutic Implications,” Clinical Neuropharmacology, Vol. 24, No. 1, 2001, pp. 43-49. doi:10.1097/00002826-200101000-00008
[8]	V. Bubeníková-Valesová, J. Horácek, M. Vrajová and C. H?schl, “Models of Schizophrenia in Humans and Animals Based on Inhibition of NMDA Receptors,” Neuroscience and Biobehavioral Reviews, Vol. 32, No. 5, 2008, pp. 1014-1023. doi:10.1016/j.neubiorev.2008.03.012
[9]	K. Y. Tseng, R. A. Chambers and B. K. Lipska, “The Neonatal Ventral Hippocampal Lesion as a Heuristic Neurodevelopmental Model of Schizophrenia,” Behavioural Brain Research, Vol. 204, No. 2, 2009, pp. 295-305. doi:10.1016/j.bbr.2008.11.039
[10]	H. P. Jedema and B. Moghddam, “Characterization of Excitatory Amino Acid Modulation of Dopamine Release in the Prefrontal Cortex of Conscious Rats,” Journal of Neurochemistry, Vol. 66, No. 4, 1996, pp. 1448-1453. doi:10.1046/j.1471-4159.1996.66041448.x
[11]	W. R. Wu, N. Li and B. A. Sorg, “Regulation of Medial Prefrontal Cortex Dopamine by Alphaamino-3-Hydroxy5-Methylisoxazole-4-Propionate/Kainate Receptors,” Neuroscience, Vol. 114, No. 2, 2002, pp. 507-516. doi:10.1016/S0306-4522(02)00276-2
[12]	C. L. Ryan, M. A. Robbins, M. T. Smith, I. C. Gallant, A. L. Adams-Marriott and T. A. Doucette, “Altered Social Interaction in Adult Rats Following Neonatal Treatment with Domoic Acid,” Physiology & Behavior, Vol. 102, No. 3-4, 2011, pp. 291-295. doi:10.1016/j.physbeh.2010.11.020
[13]	A. L. Adams, T. A. Doucette and C. L. Ryan, “Altered Pre-Pulse Inhibition in Adult Rats Treated Neonatally with Domoic Acid,” Amino Acids, Vol. 35, No. 1, 2008, pp. 157-160. doi:10.1007/s00726-007-0603-3
[14]	A. L. Marriott, C. L. Ryan and T. A. Doucette, “Neonatal Domoic Acid Treatment Produces Alterations to Prepulse Inhibition and Latent Inhibition in Adult Rats,” Pharmacology, Biochemistry and Behavior, Vol. 103, No. 2, 2012, pp. 338-344. doi:10.1016/j.pbb.2012.08.022
[15]	M. A. Burt, C. L. Ryan and T. A. Doucette, “Altered Responses to Novelty and Drug Reinforcement in Adult Rats Treated Neonatally with Domoic Acid,” Physiology & Behavior, Vol. 93, No. 1-2, 2008, pp. 327-336. doi:10.1016/j.physbeh.2007.09.003
[16]	M. A. Burt, C. L. Ryan and T. A. Doucette, “Low Dose Domoic Acid in Neonatal Rats Abolishes Nicotine Induced Conditioned Place Preference during Late Adolescence,” Amino Acids, Vol. 35, No. 1, 2008, pp. 247-249. doi:10.1007/s00726-007-0584-2
[17]	A. L. Adams, T. A. Doucette, R. James and C. L. Ryan, “Persistent Changes in Learning and Memory in Rats Following Neonatal Treatment with Domoic Acid,” Physiology & Behavior, Vol. 96, No. 4-5, 2009, pp. 505-512. doi:10.1016/j.physbeh.2008.11.019
[18]	J. M. Gold, C. Carpenter, C. Randolph, T. E. Goldberg, and D. R. Weinberger, “Auditory Working Memory and Wisconsin Card Sorting Test Performance in Schizophrenia,” Archives of General Psychiatry, Vol. 54, No. 2, 1997, pp. 159-165. doi:10.1001/archpsyc.1997.01830140071013
[19]	R. S. E. Keefe, S. E. Lees-Roitman and R. L. Dupre, “Performance of Patients with Schizophrenia on a Pen and Paper Visuospatial Working Memory Task with Short Delay,” Schizophrenia Research, Vol. 26, No. 1, 1997, pp. 9-14. doi:10.1016/S0920-9964(97)00037-6
[20]	G. W. Dalack, D. J. Healy and J. H. Meador-Woodruff, “Nicotine Dependence in Schizophrenia: Clinical Phenomena and Laboratory Findings,” The American Journal of Psychiatry, Vol., 155, No. 11, 1998, pp. 1490-1501.
[21]	R. A. Chambers and D. W. Self, “Motivational Responses to Natural and Drug Rewards in Rats with Neonatal Ventral Hippocampal Lesions: An Animal Model of Dual Diagnosis Schizophrenia,” Neuropsychopharmacology, Vol. 27, No. 6, 2002, pp. 889-905. doi:10.1016/S0893-133X(02)00365-2
[22]	B. K. Lipska, J. M. Aultman, A. Verma, D. R. Weinberger and B. Moghaddam, “Neonatal Damage of the Ventral Hippocampus Impairs Working Memory in the Rat,” Neuropsychopharmacology, Vol. 27, No. 1, 2002, pp. 47-54. doi:10.1016/S0893-133X(02)00282-8
[23]	B. Eleveg, G. D. A. Brown, T. McCormack, J. I. Vousden and T. E. Goldberg, “Identification of Tone Duration, Line Length, and Letter Position: An Experimental Approach to Timing and Working Memory Deficits in Schizophrenia,” Journal of Abnormal Psychology, Vol. 113, No. 4, 2004, pp. 509-521. doi:10.1037/0021-843X.113.4.509
[24]	B. L. Schwartz, L. H. Deutsch, C. Cohen, D. Warden and S. I. Deutsch, “Memory for Temporal Order in Schizophrenia,” Biological Psychiatry, Vol. 29, No. 4, 1991, pp. 329-339. doi:10.1016/0006-3223(91)90218-B
[25]	F. A. V. Waters, M. T. Maybery, J. C. Badcock and P. T. Michie, “Context Memory and Binding in Schizophrenia,” Schizophrenia Research, Vol. 68, No. 2-3, 2004, pp. 119-125. doi:10.1016/S0920-9964(03)00221-4
[26]	T. A. Doucette, S. M. Strain, G. V. Allen, C. L. Ryan and R. A. R. Tasker, “Comparative Behavioural Toxicity of Domoic Acid and Kainic Acid in Neonatal Rats,” Neurotoxicology and Teratology, Vol. 22, No. 6, 2000, pp. 863-869. doi:10.1016/S0892-0362(00)00110-0
[27]	T. A. Doucette, P. B. Bernard, P. C. Yuill, R. A. Tasker and C. L. Ryan, “Low Doses of Non-NMDA Glutamate Receptor agonists Alter Neurobehavioural Development in the Rat,” Neurotoxicology and Teratology, Vol. 25, No. 4, 2003, pp. 473-479. doi:10.1016/S0892-0362(03)00034-5
[28]	J. B. Mitchell and J. Laiacona, “The Medial Frontal Cortex and Temporal Memory: Tests Using Spontaneous Exploratory Behaviour in the Rat,” Behavioural Brain Research, Vol. 97, No. 1-2, 1998, pp. 107-113. doi:10.1016/S0166-4328(98)00032-1
[29]	G. Paxinos and C. Watson C, “The Rat Brain in Stereotaxic Coodinates,” 4th Editon, Academic Press, Toronto, 1998.
[30]	L. M. DeVito, R. Konigsberg, C. Lykken, M. Sauvage, W. S. Young and H. Eichenbaum, “Vasopressin 1b Receptor Knock-Out Impairs Memory for Temporal Order,” The Journal of Neuroscience, Vol. 29, No. 9, 2009, pp. 2676-2683. doi:10.1523/JNEUROSCI.5488-08.2009
[31]	J. G. Howland, R. A. Harrison, D. K. Hannesson and A. G. Phillips, “Ventral Hippocampal Involvement in Temporal Order, but Not Recognition, Memory for Spatial Information,” Hippocampus, Vol. 18, No. 3, 2008, pp. 251-257. doi:10.1002/hipo.20396
[32]	M. Akil, C. L. Edgar, J. N. Pierri, S. Casali and D. A. Lewis, “Decreased Density of Tyrosine HydroxylaseImmunoreactive Axons in the Entorhinal-Cortex of Schizophrenic Subjects,” Biological Psychiatry, Vol. 47, No. 5, 2000, pp. 361-370. doi:10.1016/S0006-3223(99)00282-6
[33]	M. Akil, J. N. Pierri, R. E. Whitehead, C. L. Edgar, C. Mohila, A. R. Sampson and D. A. Lewis, “Lamina-Specific Alterations in the Dopamine Innervation of the Prefrontal Cortex in Schizophrenic Subjects,” The American Journal of Psychiatry, Vol. 156, No. 10, 1999, pp. 1580-1589.
[34]	K. Wedzony, K. Fijal and A. Chocyk, “Blockade of NMDA Receptors in Postnatal Period Decreased Density of Tyrosine Hydroxylase Immunoreactive Axonal Arbors in the Medial Prefrontal Cortex of Adult Rats,” Journal of Physiology and Pharmacology, Vol., 56, No. 2, 2005, pp. 205-221.
[35]	A. Aguilar-Valles, C. Flores and G. N. Luheshi, “Prenatal Inflammation-Induced Hypoferremia Alters Dopamine Function in Adult Offspring in Rat: Relevance for Schizophrenia,” PloS One, Vol. 5, No. 6, 2010, e10967. doi:10.1371/journal.pone.0010967
[36]	D. J. Balfour, “Neuroplasticity within the Mesoaccumbens Dopamine System and Its Role in Tobacco Dependence,” Current Drug Targets, CNS and Neurological Disorders, Vol. 1, No. 4, 2002, pp. 413-421. doi:10.2174/1568007023339076
[37]	T. A. Doucette, C. L. Ryan and R. A. Tasker, “Genderbased Changes in Cognition and Emotionality in a New Rat Model of Epilepsy,” Amino Acids, Vol. 32, No. 3, 2007, pp. 317-322. doi:10.1007/s00726-006-0418-7
[38]	J. L. Nunez and M. M. McCarthy, “Evidence for an Extended Duration of GABA-Mediated Excitation in the Developing Male versus Female Hippocampus,” Developmental Neurobiology, Vol. 67, No. 14, 2007, pp. 1879-1890. doi:10.1002/dneu.20567
[39]	A. Kyrozis, O. Chudomel, S. L. Moshe and A. S. Galanopoulou, “Sex-Dependent Maturation of GABAA Receptor-Mediated Synaptic Events in Rat Substantia Nigra Reticulate,” Neuroscience Letters, Vol. 398, No. 1-2, 2006, pp. 1-5. doi:10.1016/j.neulet.2005.12.018
[40]	R. K. Lenroot, N. Gogtay, D. K. Greenstein, E. MolloyWells, G. L. Wallace, L. S. Clasen, J. D. Blumenthal, J. Lerch, A. P. Zijdebnos, A. C. Evans, P. M. Thompson and J. N. Giedd, “Sexual Dimorphism of Brain Developmental Trajectories during Childhood and Adolescence,” NeuroImage, Vol. 36, No. 4, 2007, pp. 1065-1073. doi:10.1016/j.neuroimage.2007.03.053