Loss of lever press-related firing of rat striatal forelimb neurons after repeated sessions in a lever pressing task

Abstract

Lateral striatal neurons that fire phasically in relation to active movement of the contralateral forelimb (determined via daily sensorimotor examination) were studied during acquisition of cued lever pressing. Rats were trained to lift the contralateral forepaw from the floor to press a lever in the presence of a tone. The tone was presented 70 times per day (session) for 18 consecutive days. All animals acquired the task, evidenced by gradual improvements across sessions and eventual asymptotic levels in tone discrimination, reaction time, and efficiency of the lever press. Forelimb neurons fired in relation to the lever press during early sessions of acquisition but not after repeated sessions on the task. This difference in firing could not be attributed to differences in forelimb movements during lever pressing or to sampling from different populations of neurons in early versus late sessions. In view of evidence that striatal damage impairs acquisition of motor skills, the change in firing suggests that the striatal activity present in early sessions may be necessary for the acquisition of, but not the automatic performance of, learned motor responses.

Fig. 1.

Schematic diagram of behavioral task and RT measures. Animals were trained to place the contralateral forepaw on a piece of tape on the floor, situated directly in front of the lever. Correct forepaw placement for 0.50–1.0 sec activated a tone, during which the animal lifted its forepaw from the tape (activation of biceps/deltoid EMG), and pressed the lever activating water delivery. See text for description of RT measures. Times are approximate means across animals and represent behavior of a trained animal. Time 0 = entry of lever into bin 3 (11 g force).

Fig. 2.

Left column, Percentage of trials in each session in which the animal responded during the tone, i.e., completed a reinforced lever press (top); completed one or more (unreinforced) lever presses during the ITI (middle); or pressed the lever beyond the force required for water delivery (bottom). Right column, RT measures (msec). RT₁ = time from onset of tone until onset of biceps or deltoid EMG activity.RT₂ = time from onset of biceps or deltoid EMG activity until onset of lever press. RT₃= time from onset of lever press until lever depression to the force required for water delivery. Asterisk indicates significant (p < 0.01) change as a function of session number (n.s., not significant).

Fig. 3.

Decline in lever press-related firing of striatal forelimb neurons after repeated sessions. Three left vertical columns, PEHs display activity of forelimb neurons and simultaneously recorded biceps and triceps EMG activity across representative sessions for one animal (166). Reinforced lever press is “node” (bin 3 entry, time 0), indicated by solid vertical lines and filled arrows (70 trials in each). Neuronal activity was time-locked to lever press during acquisition (e.g., sessions 4 and 5, the latter yielding neurons) but not after repeated sessions (e.g., 9 and 12). Timing of onset of biceps/triceps EMG activity remained similar across sessions (amplitude was not quantified; 2 msec/bin). Vertical column toright of dashed line, PEHs show responsiveness of each neuron at far left to cutaneous stimulation during exam before session (60 repetitions of tapping or rubbing limb/paw, indicated by solid vertical line andopen arrow; 4 msec/bin).

Fig. 4.

Decline in lever press-related firing of forelimb neurons after repeated sessions in a different animal (171). Firing was time-locked to the reach toward lever during acquisition (e.g., sessions 2, 5, and 7) but not after repeated sessions (e.g., 14 and 18). Onset of biceps/deltoid EMG activity was similar across sessions. Secondary peaks in neuronal activity and EMG activity at −0.50 sec reflect residual from ITI lever presses, which persisted at three to four per ITI for this animal. Details as in Figure 3,left.

Fig. 5.

S:B across all sessions for each animal (animalnumber at top). Each vertical bar represents S:B for one forelimb neuron. Ratio near 1 (dashed horizontal line) indicates that firing rate did not change as the paw moved from position on tape to reach and press the lever. Asterisk indicates significant (p < 0.01) change in S:B as a function of session number. Inset, Similar trend in S:B as a function of session number obtained from two animals in the initial study.