JBBS  Vol.4 No.5 , May 2014
Basolateral Amygdala Inactivation Reduces Sexual Motivation in Male Rats during Performance of a T-Maze Task with a Sexual Reward
Abstract: This study was aimed to determine the effect of amygdaline inactivation on the sexual motivation of male rats during a T-maze task with a sexual reward. Subjects were chronically implanted with two stainless-steel cannulae that enabled the infusion of tetrodotoxin, a sodium channel blocker, into the left and right basolateral amygdala (BLA). Animals were divided into 3 groups: saline (SS); TTX1 (tetrodotoxin at 2.5 ng); and TTX2 (tetrodotoxin at 5.0 ng). To induce a sexually-motivated state, all male rats were allowed to have an intromission with a receptive female before performing the T-maze task, after which their sexual motivation was evaluated during seven trials in which a receptive female was placed in one goal-box of the T-maze, and a non-receptive one in the other. Subjects were allowed an intromission as a sexual reward whenever they reached the goal-box containing the receptive female, but were returned to the start-box if they did not. At the end of the experiment, copulation until ejaculation was permitted. Both doses of TTX increased the time rats required to cross the maze stem during the final trials. In terms of sexual interaction, the high dose of TTX increased more markedly mount, intromission and ejaculation latencies and the number of mounts and intromissions. Overall, these results indicate that the BLA may play an important role in modulating sexual behavior, particularly in maintaining sexual motivation in successive trials in a T-maze task and during sexual interaction per se.
Cite this paper: Hernández-González, M. , Aguirre, F. , Guevara, M. , Quirarte, G. and Magallanes, P. (2014) Basolateral Amygdala Inactivation Reduces Sexual Motivation in Male Rats during Performance of a T-Maze Task with a Sexual Reward. Journal of Behavioral and Brain Science, 4, 223-233. doi: 10.4236/jbbs.2014.45024.

[1]   McDonald, A. (2003) Is There an Amygdala and How Far Does It Extend? An Anatomical Perspective. Annual NY Academy of Science, 985, 1-21.

[2]   Pitkänen, A. (2000) Connectivity of the Rat Amygdaloid Complex. In: Aggleton, J.P., Ed., The Amygdala, Oxford University Press, New York, 31-115.

[3]   Gloor, P. (1997) The Amygdaloid System. In: Gloor, P., Ed., The Temporal Lobe and Limbic System, Oxford University Press, New York, 591-721.

[4]   Price, J.L., Russchen, E.T. and Amaral, D.G. (1987) The Amygdaloid Complex. In: Björklund, A., Hökfelt, T. and Swanson, L.W., Eds., Handbook of Chemical Neuroanatomy, Volume 5, Integrated systems of the CNS, Part 1, Elsevier, Amsterdam, 279-388.

[5]   Alheid, G.F. and Heimer, L. (1988) New Perspectives in Basal Forebrain Organization of Special Relevance for Neuropsychiatric Disorders: The Striatopalidal, Amygdaloid, and Corticopetal Components of Substantia Innominata. Neuroscience, 27, 1-39.

[6]   McDonald, A. (1998) Cortical Pathways to the Mammalian Amygdala. Progress in Neurobiology, 55, 257-332.

[7]   Swanson, L.W. and Petrovich, G.D. (1998) What Is the Amygdala? Trends in Neuroscience, 21, 323-333.

[8]   Cardinal, R.N., Parkinson, J.A., Hall, J. and Everitt, B.J. (2002) Emotion and Motivation: The Role of the Amygdala, Ventral Striatum and Prefrontal Cortex. Neuroscience Biobehavioral Review, 26, 321-352.

[9]   G. Schoenbaum, Chiba, A. and Gallagher, M. (1998) Orbitofrontal Cortex and Basolateral Amygdala Encode Expected Outcomes during Learning. Nature Neuroscience, 1, 155-159.

[10]   Hatfield, T., Han, J., Conley, M., Gallagher, M. and Holland, P. (1997) Neurotoxic Lesions of Basolateral, But Not Central, Amygdala Interfere with Pavlovian Second-Order Conditioning and Reinforce Devaluation Effects. The Journal of Neuroscience, 17, 6011-6020.

[11]   Gaffan, D. and Murray, A.E. (1990) Amygdalar Interaction with the Mediodorsal Nucleus of the Thalamus and the Ventro-Medial Prefrontal Cortex in Stimulus-Reward Associative Learning in the Monkey. The Journal of Neuroscience, 10, 3479-3493.

[12]   Izquierdo, A. and Murray, E.A. (2004) Combined Unilateral Lesions of the Amygdala and Orbital Prefrontal Cortex Impair Affective Processing in Rhesus Monkeys. Journal of Neurophysiology, 91, 2023-2039.

[13]   Baxter, M.G., Parker, A., Lindner, C.C., Izquierdo, A.D. and Murray, E.A. (2000) Control of Response Selection by Reinforcer Values Requires Interaction of Amygdala and Orbitofrontal Cortex. The Journal of Neuroscience, 20, 4311-4319.

[14]   Schoenbaum, G., Chiba, A. and Gallagher, M. (2000) Changes in Functional Connectivity in Orbitofrontal Cortex and Basolateral Amygdala during Learning and Reversal Training. The Journal of Neuroscience, 20, 5179-5189.

[15]   Schoenbaum, G., Setlow, B., Nugent, S., Saddoris, M. and Gallagher, M. (2003) Lesions of Orbitofrontal Cortex and Basolateral Amygdala Complex Disrupt Acquisition of Odor-Guided Discriminations and Reversals. Learning and Memory, 10, 129-140.

[16]   Schoenbaum, G., Setlow, B., Saddoris, M. and Gallagher, M. (2003) Encoding Predicted Outcome and Acquired Value in Orbitofrontal Cortex during Cue Sampling Depends upon Input from Basolateral Amygdala. Neuron, 39, 855-867.

[17]   Baxter, M.G. and Murray, E.A. (2002) The Amygdala and Reward. Nature Reviews Neuroscience, 3, 563-573.

[18]   Sheffield, F.D., Wulff, J.J., and Backer, R.R. (1951) Reward Value of Copulation without Sexual Drive Reduction. Journal of Comparative and Physiological Psychology, 44, 3-8.

[19]   Sheffield, F.D., Roby, T.B. and Campbell, B.A. (1954) Drive Reduction versus Consummatory Behavior as Determinants of Reinforcement. Journal of Comparative and Physiological Psychology, 47, 349-354.

[20]   Denniston, R.H. (1954) Quantification and Comparation of Sex Drives under Various Conditions in Terms of Learned Responses. Journal of Comparative and Physiological Psychology, 47, 437-440.

[21]   Kagan, J. (1955) Differential Reward Value of Incomplete and Complete Sexual Behaviour. Journal of Comparative and Physiological Psychology, 48, 59-64.

[22]   Everitt, B.J., Fray, P., Kostarczyk, E., Taylor, S. and Stacey, P. (1987) Studies of Instrumental Behavior with Sexual Reinforcement in Male Rats (Rattus norvegicus): I. Control by Brief Visual Stimuli Paired with a Receptive Female. Journal of Comparative Psychology, 101, 395-406.

[23]   Jowaisas, D., Taylor, J., Dewsbury, D.A. and Malagodi, E.F. (1971) Copulatory Behavior of Male Rats under an Imposed Operant Requirement. Psychonomic Science, 25, 287-290.

[24]   Beach, F.A. and Jordan, L. (1956) Effects of Sexual Reinforcement upon the Performance of Male Rats in a Straight Runway. Journal of Comparative and Physiological Psychology, 49, 105-110.

[25]   Whalen, R.E., Beach, F.A. and Kuehn, R.E. (1961) Effects of Exogenous Androgen on Sexually Responsive and Unresponsive Male Rats. Endocrinology, 68, 373-380.

[26]   Everitt, B.J. and Stacey, P. (1987) Studies of Instrumental Behavior with Sexual Reinforcement in Male Rats (Rattus norvegicus): II. Effects of Preoptic Area Lesions, Castration, and Testosterone. Journal of Comparative Psychology, 101, 407-419.

[27]   Hetta, J. and Meyerson, B.J. (1978) Sexual Motivation in the Male Rat: A Methodological Study of Sex-Specific Orientation and the Effects of Gonadal Hormones. Acta Physiologica Scandinavica Supplementum, 453, 1-67.

[28]   López, H.H. and Ettenberg, A. (2001) Dopamine Antagonism Attenuates the Unconditioned Incentive Value of Estrous Female Cues. Pharmacology and Biochemical Behavior, 68, 411-416.

[29]   Hernández-González, M., Prie-to-Beracoechea, C.A., Arteaga-Silva, M. and Guevara, M.A. (2007) Different Functionality of the Medial and Orbital Prefrontal Cortex during a Sexually Motivated Task in Rats. Physiology & Behavior, 90, 450-458.

[30]   Sachs, B.D. and Barfield, R.J. (1976) Functional Analysis of Masculine Copulatory Behavior in the Rat. In: Hinde, R. A., Shaw, E. and Beer, C., Eds., Advances in the Study of Behaviour, Vol. 7, Academic Press, New York, 91-154.

[31]   Kurtz, R. and Adler, N. (1973) Electrophysiological Correlates of Copulatory Behavior in the Male Rat: Evidence for a Sexual Inhibitory Process. Journal of Comparative and Physiological Psychology, 84, 225-239.

[32]   Harris, V.S. and Sachs, B.D. (1975) Copulatory Behavior in Male Rats Following Amygdaloid Lesions. Brain Research, 86, 514-518.

[33]   Kondo, S. (1992) Lesions of the Medial Amygdala Produce Severe Impairment of Copulatory Behavior in Sexually Inexperienced Male Rats. Physiology & Behavior, 51, 939-943.

[34]   McGregor, A. and Herbert, J. (1992) Differential Effects of Excitotoxic Basolateral and Corticomedial Lesions of the Amygdala on the Behavioural and Endocrine Responses to Either Sexual or Aggression-Promoting Stimuli in the Male Rat. Brain Research, 574, 9-20.

[35]   Lehman, M.N. and Winans, S.S. (1982) Vomeronasal and Olfactory Pathways to the Amygdala Controlling Male Hamster Sexual Behavior: Autoradiographic and Behavioral Analyses. Brain Research, 240, 27-41.

[36]   Everitt, B.J., Cador, M. and Robbins, T.W. (1989) Interactions between the Amygdala and Ventral Striatum in Stimulus-Reward Associations: Studies Using a Second-Order Schedule of Sexual Reinforcement. Neuroscience, 30, 63-75.

[37]   Everitt, B.J., Cardinal, R.N., Parkinson, J.A. and Robbins, T.W. (2003) Appetitive Behavior: Impact of Amygdala Dependent Mechanisms of Emotional Learning. Annual New York Academy of Science, 985, 233-250.

[38]   Kippin, T.E., Cain, S.W. and Pfaus, J.G. (2003) Estrous Odors and Sexually Conditioned Neutral Odors Activate Separate Neural Pathways in the Male Rat. Neuroscience, 117, 971-979.

[39]   Moncho-Bogani, J., Martinez-Garcia, F., Novejarque, A. and Lanuza, E. (2005) Attraction to Sexual Pheromones and Associated Odorants in Female Mice Involves Activation of the Reward System and Basolateral Amygdala. European Journal of Neuroscience, 21, 2186-2189.

[40]   De Jonge, F.H., Tonnaer, J.A., Van Leeuwe, H., Tielemans, A.J., Louwerse, A.L. and Van de Poll, N.E. (1992) Cerebral Glucose Utilization during Conditioned Sexual Arousal. Physiology and Behavior, 52, 1009-1013.

[41]   Magyar, O., Hill, M.N., Pinel, J.P. and Gorzalka, B.B. (2005) Long-Term Kindling of the Basolateral Amygdala Impairs Copulatory Behavior in Male Rats. Neuroscience Letters, 390, 162-165.

[42]   Paxinos, G. and Watson, C. (1997) The Rat Brain in Stereotaxic Coordinates. Academic Press, New York.

[43]   Guevara, M.A., Robles-Aguirre, F.A., Quirarte, G.L. and Hernández-González, M. (2009) Orbitofrontal Cortex Inactivation Impairs Early Reversal Learning in Male Rats during a Sexually Motivated Task. International Journal of Psychology and Psychological Therapy, 9, 141-160.

[44]   Bielawska, E. and Roldan, G. (1996) Ipsilateral Connections between the Gustatory Cortex, Amygdala and Parabrachial Nucleus are Necessary for Acquisition and Retrieval of Conditioned Taste Aversion in Rats. Behavioural Brain Research, 81, 25-31.

[45]   Boehnke, S. and Rasmusson, D. (2001) Time Course and Effective Spread of Lidocaine and Tetrodotoxin Delivered via Microdialysis: An Electrophysiological Study in Cerebral Cortex. Journal of Neuroscience Methods, 105, 133-141.

[46]   Ali-Vafaei, A. and Rashidy-Pour, A. (2004) Reversible Lesion of the Rat’s Orbitofrontal Cortex Interferes with Hippocampus-Dependent Spatial Memory. Behavioral Brain Research, 149, 61-68.

[47]   Kilpatrick, L. and Cahill, L. (2003) Modulation of Memory Consolidation for Olfactory Learning by Reversible Inactivation of the Basolateral Amygdala. Behavioral Neuroscience, 117, 184-188.

[48]   Quiroz, C., Martínez, I., Quirarte, G.L., Morales, T., Díaz-Cintra, S. and Prado-Alcalá, R. (2003) Enhanced Inhibitory Avoidance Learning Prevents the Memory-Impairing Effects of Posttraining Hippocampal Inactivation. Experimental Brain Research, 221, 400-422.

[49]   Lorenzini, A., Baldi, E., Bucherelli, C., Sacchetti, B. and Tassoni, G. (1997) Analysis of Mnemonic Processing by Means of Totally Reversible Inactivations. Brain Research Protocols, 1, 391-398.

[50]   Ågmo, A. (1999) Sexual Motivation—An Inquiry into Events Determining the Ocurrence of Sexual Behavior. Behavioural Brain Research, 105, 129-150.

[51]   Ågmo, A. (2002) Copulation-Contingent Aversive Conditioning and Sexual Incentive Motivation in Male Rats: Evidence for a Two-Stage Process of Sexual Behavior. Physiology & Behavior, 77, 425-435.

[52]   Pfaff, D.W. and Ågmo, A. (2002) Reproductive Motivation. In: Gakkistel, R. and Pashler, H., Eds., Steven’s Handbook of Experimental Psychology: Learning, Motivation and Emotion, Vol. 3, John Wiley and Sons, New York, 709-736.

[53]   Balleine, B.W., Killcross, S. and Dickinson, A. (2003) The Effect of Lesions of the Basolateral Amygdala on Instrumental Conditioning. The Journal of Neuroscience, 23, 666-675.

[54]   Balleine, B.W. and Dickinson, A. (1998) Goal-Directed Instrumental Action: Contingency and Incentive Learning and Their Cortical Substrates. Neuropharmacology, 37, 407-419.

[55]   Ågmo, A., Villalpando, A., Picker, Z. and Fernández, H. (1995) Lesions of the Medial Prefrontal Cortex and Sexual Behavior in the Male Rat. Brain Research, 9, 177-186.

[56]   Pfaus, J.G. (1999) Neurobiology of Sexual Behavior. Current Opinion in Neurobiology, 9, 751-758.

[57]   Hull, E.M., Meisel, R.L. and Sachs B.D. (2002) Male Sexual Behavior. In: Pfaff, D.W., Arnold, A.P., Etgen, A.M., Fahrbach, S.E. and Rubin, R.T., Eds., Hormones, Brain and Behavior, Academic Press, Waltham, 3-137.

[58]   Sachs, B.D. (2000) Contextual Approaches to the Physiology and Classification of Erectile Function, Erectile Dysfunction, and Sexual Arousal. Neuroscience & Biobehavioral Review, 24, 541-560.

[59]   Pfaus, J.G., Kipping, T.E. and Coria-Avila, G. (2003) What Can Animal Models Tell Us about Human Sexual Response? Annual Review of Sex Research, 14, 1-63.

[60]   Turner, B.H. (1973) Sensorimotor Syndrome Produced by Lesions of the Amygdala and Lateral Hypothalamus. Journal of Comparative and Physiological Psychology, 82, 37-47.