The role of the pedunculopontine tegmental nucleus in relation to conditioned motor performance in the cat

Abstract

The activity of the pedunculopontine tegmental nucleus (PPTg) neurons was recorded in three unrestrained cats operantly conditioned to perform a lever-release movement. The movement had to be initiated either rapidly after a (click) stimulus in a simple reaction-time paradigm or had to be delayed after the same stimulus in trials identified by a tone cue. Successful trials were rewarded by a food pellet. A total of 107 neurons were recorded with microelectrodes. Brief spike neurons (mean duration: 0.7 ms) and broad spike neurons (mean duration: 2 ms) presumed to be cholinergic were detected. Of the 73 neurons localized in the PPTg area, 53 had brief spikes and 20 broad spikes. Changes in activity most commonly occurred very early after the stimulus or during the reinforcement process. Most neurons with brief spikes exhibited very early excitation after the stimulus and reinforcement-related activity. These neurons had a mean activity of 23.7 impulses/s in the period preceding the stimulus. The onset of activation after the stimulus had a latency of 8.6+/-6.9 ms (mean+/-SD), with a range of 4-35 ms. In trials where the movement had to be delayed after the stimulus, the early activation disappeared or was considerably reduced, showing that it was context-dependent. A small proportion of neurons with brief spikes initially decreased activity after the stimulus, but with a latency >9 ms. All the neurons with broad spikes, except one, had reinforcement-related activity. Half of them showed exclusively reinforcement-related activity, the other half also early activation after the stimulus. These neurons were about half as active in the period preceding the stimulus occurrence than the neurons with brief spikes. The early context-dependent activation is discussed in relation to the excitatory projection of PPTg neurons on the subthalamic nucleus. The reinforcement-related activity, preferentially evidenced in broad spike neurons presumed to be cholinergic, is speculated to be associated with cholinergic projection of PPTg neurons to the dopaminergic neurons of the substantia nigra. Finally, the role of PPTg in the ongoing control of motor performance and reinforcement processes is discussed in relation to the basal ganglia circuitry.

Imagined gait modulates neuronal network dynamics in the human pedunculopontine nucleus

“…Cholinergic neurons are more prevalent in the caudal PPN, and the presence of gait disorders has been correlated with loss of these cells [14][15][16] . As wide-spike neurons had a significantly lower density than narrow-spike neurons, and were more common in the caudal PPN, these cells are likely to be cholinergic neurons 40 .…”

“…Cholinergic neurons are more prevalent in the caudal PPN, and the presence of gait disorders has been correlated with loss of these cells [14][15][16] . As wide-spike neurons had a significantly lower density than narrow-spike neurons, and were more common in the caudal PPN, these cells are likely to be cholinergic neurons 40 .Limb movement and imagined gait had diverse effects on neural activity in the PPN 33 , but resulted in an overall reduction in activity. The PPN has extensive connections with the basal ganglia 5, 11 , receiving strong inhibitory inputs from both the globus pallidus internus and substantia nigra 41 .…”

Reward Prediction Error Computation in the Pedunculopontine Tegmental Nucleus Neurons

“…The reward delivery neurons may receive the actual reward signals from the lateral hypothalamus (Rolls et al, 1980;Fukuda et al, 1986;. This pathway directly excites the PPTN (Semba & Fibiger, 1992), which responds with a brief burst and then accommodates or habituates (Takakusaki et al, 1997;Dormont et al, 1998). This brief burst, in turn, directly excites the midbrain dopamine neurons via cholinergic and glutamatergic projections (Conde, 1992) and thereby causes a phasic burst in dopamine neurons projecting to the striatum (Gerfen, 1992) for actual reward.…”

“…A number of studies have found impairments in learning following excitotoxic lesions of the PPTN (Fujimoto et al, 1989;Fujimoto et al, 1992;Steckler et al, 1994;Inglis et al, 2000;Alderson et al, 2002). Thus, abundant anatomical, electrophysiological and pharmacological studies of slice and whole animal preparations indicate that the PPTN receives signals from the reward related structures including the cerebral cortices and the striatum (Winn et al, 1997) and provides strong excitatory inputs to the dopamine neurons (Clements & Grant, 1990;Blaha & Winn, 1993;Futami et al, 1995;Oakman et al, 1995;Blaha et al, 1996;Conde et al, 1998;Dormont et al, 1998;MenaSegovia et al, 2004;Pan & Hyland, 2005;Mena-Segovia et al, 2008). Interestingly, the dopamine/ acethylcholine interaction seems to be mutual (Scarnati et al, 1987); dopmine neurons in the substantia nigra pars compacta tproject back to PPTN neurons, affecting their excitability.…”

Participation of the pedunculopontine tegmental nucleus in arousal-demanding functions

“…They have a key role in attention and sensory processes that are needed for proper selection of motor responses to stimuli that are of behavioral significance [111][112][113][114]. Because PPTg neurons also respond to the presentation of stimuli of behavioral significance [115,116], the striatum may process behavior-related signals carried through the PPTg-Pf pathway. The excitatory neurons that form this pathway would ensure a fast route for the conduction of sensory information to the striatum.…”