Uncontrollable shock, forebrain norepinephrine, and stimulus selection during choice-escape learning

Abstract

Exposure to uncontrollable shock impairs later choice-escape learning in rats. A deficit occurs only when an irrelevant cue is presented on choice trials and the rat is unable to ignore the cue. Three experiments examined the role of stress-induced depletion of forebrain norepinephrine (NE) in the choice-accuracy deficit. Experiments 1 and 2 established a relationship between stressfulness of pretreatment sessions, magnitude of the deficit in later choice escape, and depletion of forebrain NE upon reexposure to a few shocks 24 h after pretreatment. Experiment 3 established that NE depletion is sufficient to impair choice performance. Bilateral 6-hydroxydopamine lesions of the ascending dorsal tegmental bundle mimicked the effects of inescapable shock. Lesioned rats showed a deficit in choice accuracy only when an irrelevant cue was presented during choice testing. Vehic1e controls were unimpaired regardless of cue condition. These data are consistent with the notion that the ascending dorsal tegmental bundle is involved in attentionlike processing and suggest that deficits in stimulus selection following inescapable shock may result from stress-induced depletion of forebrain NE.Although it is weIl established that exposure to inescapable, but not to escapable, eleetric shock impairs later escape performance in rats (Maier, Albin, & Testa, 1973; Seligman, Rosellini, & Kozak, 1975), there is stilliittie agreement concerning the mechanism underlying this effeet. Maier and Seligman (1976) argue that rats learn that their behavior and shock termination during inescapable shock are unrelated, and therefore that responding will be ineffective in producing future outcomes. This expectation of helplessness generalizes to the test task to produce cognitive, motivational, and emotional impairment. Alternatively, deficits in escape performance following inescapable shock could reflect a reduced capacity to respond. Activity deficits could arise from stress-induced depletion ofbrain catecholamines (

Individual differences in vulnerability to inescapable shock in rats.

“…Similar percentages in explained variance were obtained in Experiments 1 and 2 with the shuttle-escape measure (54%) and saccharin finickiness (48%). These data confirm and extend the finding that pretreatment stressor severity is a critical extrinsic modulator of distress and helplessness (Anisman & Zacharko, 1986; Looney & Cohen, 1972; Minor, Pelleymounter, & Maier, 1988). At the same time, however, the experimental variable does not explain about 50% of the variance in these test measures.…”

“…Escape latency increased across preshock conditions to a point at which most individuals in the 120-shock group showed severe impairment of escape performance. This substantial effect concurs with findings from related studies on stressor severity (Anisman & Zacharko, 1986; Looney & Cohen, 1972; Minor, Pelleymounter, & Maier, 1988). Nonetheless, only 49% of the variance in escape latencies was accounted for by the number of preshocks.…”

Stress and adenosine: II. Adenosine analogs mimic the effect of inescapable shock on shuttle-escape performance in rats.

“…Previous research has shown that comparatively mild stressors provoke excessive neural activation in several transmitter systems and brain regions in rats preexposed to inescapable shock 24 hr earlier (Anisman & Zacharko, 1986;Minor, Pelleymounter, & Maier, 1988; J. M. Weiss et al, 1981). This reaction to test stimuli resembles the conditions under which adenosine is liberated into the extracellular space as a compensatory reaction to rapid energy expenditure produced by excessive neural excitation (Ames, Li, Heher, & Kimble, 1992;Fredholm & Dunwiddie, 1988;Rail, 1990;Meghji, 1991;Newby, 1984;Stone & Bartrup, 1991).…”

Effects of signaling inescapable shock on subsequent escape learning: Implications for theories of coping and "learned helplessness."

“…Pavlovian cues may modulate the chronicity of the arousal in these systems during pretreatment. Moreover, reexposure to Pavlovian fear cues during testing could rapidly reactivate these already taxed neural systems (e.g., Minor, Pelleymounter, & Maier, 1988; Weiss & Simson, 1985). The long-term effect of chronic activation of these neural substrates during pretreatment and testing could result in the neural chemical changes that are frequently observed in inescapably shocked subjects (e.g., Anisman & Sklar, 1979; Hallhammer, Bell, Ludwig, & Rea, 1983; Weiss et al, 1981).…”