Nicotine and methamphetamine disrupt habituation of sensory reinforcer effectiveness in male rats

Abstract

The reinforcing effectiveness of a sensory stimulus such as light-onset rapidly habituates (Lloyd, Gancarz, Ashrafioun, Kausch, & Richards, 2012). According to memory-based theories, habituation occurs if a memory exists for perceived stimulation, and dishabituation occurs if a memory does not exist and the stimulation is "unexpected." According to Redgrave and Gurney (2006), unexpected response-contingent sensory stimuli increase phasic firing of dopamine neurons, providing a sensory error signal that reflects the difference between perceived and expected stimuli. Together, memory-based theories of habituation and the sensory error signal hypothesis predict a disruption (slowing) of habituation rate by novel response-contingent sensory stimulation or by artificial increases in dopamine neurotransmission by stimulant drugs. To test these predictions, we examined the effects of stimulant drugs on both the operant level of responding (snout-poking) and operant responding for a sensory reinforcer (light-onset) presented according to a fixed ratio 1 schedule. Robust within-session decreases in responding indicating habituation were observed. The effects of stimulant drugs (saline, n = 10; nicotine, 0.40 mg/kg, n = 10; and methamphetamine, 0.75 mg/kg, n = 9) on habituation in rats were determined. Nicotine was found to decrease habituation rate and did not affect response rate, while methamphetamine decreased habituation rate and increased response rate. In addition, introduction of a novel visual stimulus reinforcer decreased habituation rate and increased responding. These findings show that habituation of reinforcer effectiveness modulates operant responding for sensory reinforcers, and that stimulant drugs may disrupt normally occurring habituation of reinforcer effectiveness by increasing dopamine neurotransmission.

Figure 1

Comparison of the changes in snout poking responding between the first 5-session block of the Operant Level phase (Block 1) and the second 5-session block of the Operant Level phase (Block 2). The left column of Figure 1 shows within-session responding during the Operant Level phase plotted in 8-min epochs. The right column shows habituation rate. Asterisks indicate significant p < .05.

Figure 2

The effects of drug treatment on the habituation rate during the 10-session Drug Alone phase were compared with habituation rate during the last 5-session block of the Operant Level phase. The left column of Figure 2 shows within-session responding during the Operant Level phase plotted in 8-min epochs. The right column shows habituation rate. The top row (A) shows results from saline (SAL)-treated rats, the middle row (B) shows results from nicotine (NIC, 0.4 mg/kg)-treated rats, and the bottom row (C) shows results from methamphetamine (METH, 0.75 mg/kg)-treated rats. Asterisks indicate significant p < .05.

Figure 3

Effects of response-contingent light-onset on habituation rate and responding were compared with habituation rate and responding during Block 4 of the Drug Alone phase. The left column of Figure 3 shows within-session active responding during the Operant Level phase plotted in 8-min epochs. The middle column of Figure 3 shows within-session inactive responding during the Operant Level phase plotted in 8-min epochs. The right column shows habituation rate. The top row (A) shows results from saline (SAL)-treated rats, the middle row (B) shows results from nicotine (NIC, 0.4 mg/kg)-treated rats, and the bottom row (C) shows results from methamphetamine (METH, 0.75 mg/kg)-treated rats. Asterisks indicate significant p < .05.