Role of gustatory thalamus in anticipation and comparison of rewards over time in rats.

Rats reduce intake of a palatable saccharin solution when it is followed by access to a preferred sucrose solution. This phenomenon, referred to as an anticipatory contrast effect (ACE), is thought to occur because the value of the saccharin conditioned stimulus pales in comparison to the highly rewarding sucrose unconditioned stimulus expected in the near future. Although relatively little is known about the underlying neural substrates, lesions of the gustatory thalamus fully disrupt the phenomenon (Reilly S, Bornovalova M, and Trifunovic R. Behav Neurosci 118: 365-376, 2004; Reilly S and Pritchard TC. Behav Neurosci 110: 746-759, 1996). The present set of experiments revisited this issue to determine the nature of this deficit. Rats with bilateral ibotenic acid lesions of the gustatory thalamus were given 3-min access to 0.15% saccharin and, after a 0-s or 5-min interval, were given 3-min access to either the same saccharin solution or a highly preferred 1.0 M sucrose solution. In experiment 1, ACE testing began with the 5-min interstimulus interval (ISI) and then switched to the 0-s ISI. For experiment 2, the order of ISI testing was reversed. The results show that axon-sparing, neurotoxic lesions of the gustatory thalamus prevent ACEs with a 0-s ISI and lead to a reversal (i.e., a reinforcement effect) with a 5-min ISI. Together, the results suggest that the lesion leads to a specific reward comparison deficit, whereby the rats fail to compare the value of an available reward with the memory of a preferred reward that is anticipated in the near future.

[1]  H. T. Blair,et al.  Anticipatory head direction signals in anterior thalamus: evidence for a thalamocortical circuit that integrates angular head motion to compute head direction , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[2]  S. Reilly,et al.  Gustatory thalamus lesions in the rat: II. Aversive and appetitive taste conditioning. , 1996, Behavioral neuroscience.

[3]  C. Pfaffmann,et al.  Electrophysiologically monitored lesions in the gustatory thalamic relay of the albino rat. , 1962, Journal of Comparative and Physiological Psychology.

[4]  C. Flaherty,et al.  Bidirectional contrast as a function of rate of alternation of two sucrose solutions , 1974 .

[5]  C. Flaherty,et al.  Temporal dynamics of corticosterone elevation in successive negative contrast , 1998, Physiology & Behavior.

[6]  G. A. Rowan,et al.  Chlordiazepoxide and the determinants of negative contrast , 1986 .

[7]  A. Sclafani,et al.  Qualitative differences in polysaccharide and sugar tastes in the rat: A two-carbohydrate taste model , 1987, Neuroscience & Biobehavioral Reviews.

[8]  G. A. Rowan,et al.  Effect of intersolution interval, chlordiazepoxide, and amphetamine on anticipatory contrast , 1988 .

[9]  S. Reilly,et al.  Gustatory Thalamus Lesions in the Rat: III. Simultaneous Contrast and Autoshaping , 1997, Physiology & Behavior.

[10]  C. Flaherty,et al.  Investigation of the devaluation interpretation of anticipatory negative contrast. , 1995, Journal of experimental psychology. Animal behavior processes.

[11]  C. Flaherty,et al.  Deprivation state and temporal horizons in anticipatory contrast. , 1991 .

[12]  G. Paxinos The Rat nervous system , 1985 .

[13]  G A Lucas,et al.  Anticipation of future food: suppression and facilitation of saccharin intake depending on the delay and type of future food. , 1990, Journal of experimental psychology. Animal behavior processes.

[14]  Ralph Norgren,et al.  25 – Gustatory System , 1990 .

[15]  P. S. Grigson,et al.  Microstructural analysis of successive negative contrast in free-feeding and deprived rats , 1993, Physiology & Behavior.

[16]  S. Reilly,et al.  Excitotoxic lesions of the gustatory thalamus spare simultaneous contrast effects but eliminate anticipatory negative contrast: evidence against a memory deficit. , 2004, Behavioral neuroscience.

[17]  G. A. Rowan,et al.  Anticipatory contrast: Within-subjects analysis , 1985 .

[18]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[19]  O. L. Tinklepaugh An experimental study of representative factors in monkeys. , 1928 .

[20]  Clifford B. Saper,et al.  Subnuclear organization of the efferent connections of the parabrachial nucleus in the rat , 1984, Brain Research Reviews.

[21]  A. Sclafani Starch and sugar tastes in rodents: An update , 1991, Brain Research Bulletin.

[22]  P. S. Grigson,et al.  Bilateral lesions of the gustatory thalamus disrupt morphine- but not LiCl-induced intake suppression in rats: evidence against the conditioned taste aversion hypothesis , 2000, Brain Research.

[23]  H. Grill,et al.  Reward comparison in chronic decerebrate rats. , 1997, The American journal of physiology.

[24]  C. Flaherty,et al.  Anticipation of incentive gain , 1982 .

[25]  S. Reilly,et al.  Gustatory thalamus lesions in the rat: I. Innate taste preferences and aversions. , 1996, Behavioral neuroscience.

[26]  C. Flaherty Incentive contrast: A review of behavioral changes following shifts in reward , 1982 .

[27]  R. A. Wheeler,et al.  Chronic morphine treatment exaggerates the suppressive effects of sucrose and cocaine, but not lithium chloride, on saccharin intake in Sprague-Dawley rats. , 2001, Behavioral neuroscience.

[28]  H. Grill,et al.  Central gustatory lesions: II. Effects on sodium appetite, taste aversion learning, and feeding behaviors. , 1991, Behavioral neuroscience.

[29]  C. Flaherty,et al.  Correlation of corticosterone elevation and negative contrast varies as a function of postshift day , 1985 .

[30]  P. S. Grigson,et al.  Gustatory functions, sodium appetite, and conditioned taste aversion survive excitotoxic lesions of the thalamic taste area. , 1997, Behavioral neuroscience.

[31]  C. Flaherty,et al.  Conditions under which chlordiazepoxide influences gustatory contrast , 2004, Psychopharmacology.

[32]  R. Norgren Taste pathways to hypothalamus and amygdala , 1976, The Journal of comparative neurology.

[33]  C. Flaherty,et al.  From contrast to reinforcement: role of response contingency in anticipatory contrast. , 1988, Journal of experimental psychology. Animal behavior processes.

[34]  G A Lucas,et al.  Journal of the Experimental Analysis of Behavior Time Horizons in Rats: the Effect of Operant Control of Access to Future Food , 2022 .

[35]  C. Flaherty,et al.  Within-subjects positive and negative contrast effects in rats. , 1975, Journal of comparative and physiological psychology.

[36]  C. Saper,et al.  Efferent connections of the parabrachial nucleus in the rat , 1980, Brain Research.

[37]  T. Ono,et al.  Retrospective and prospective coding for predicted reward in the sensory thalamus , 2001, Nature.

[38]  G. A. Rowan,et al.  Successive, simultaneous, and anticipatory contrast in the consumption of saccharin solutions. , 1986, Journal of experimental psychology. Animal behavior processes.

[39]  H. Grill,et al.  Gustatory cortex in the rat. II. Thalamocortical projections , 1986, Brain Research.

[40]  S. Reilly,et al.  Gustatory thalamus lesions eliminate successive negative contrast in rats: evidence against a memory deficit. , 2003, Behavioral neuroscience.

[41]  Decremental carryover effects of sucrose ingestion in the negative anticipatory contrast procedure in rats. , 1995 .

[42]  M. Taussig The Nervous System , 1991 .

[43]  H. Grill,et al.  Central gustatory lesions: I. Preference and taste reactivity tests. , 1991, Behavioral neuroscience.

[44]  Anticipatory contrast as a function of access time and spatial location , 1996 .

[45]  William Timberlake,et al.  Anticipatory contrast as a measure of time horizons in the rat: Some methodological determinants , 1988 .

[46]  S. J. Gatley,et al.  Decreased striatal dopaminergic responsiveness in detoxified cocaine-dependent subjects , 1997, Nature.

[47]  G. A. Rowan,et al.  Selective breeding for negative contrast in consummatory behavior. , 1994, Journal of experimental psychology. Animal behavior processes.

[48]  R. Norgren Gustatory afferents to ventral forebrain. , 1974, Brain research.

[49]  C. Flaherty,et al.  Relative hedonic value modulates anticipatory contrast , 1994, Physiology & Behavior.