Medullary reticular formation activity during ingestion and rejection in the awake rat

Abstract

The consummatory components of ingestion and rejection, organized in the caudal brainstem, include licking, swallowing, and the oral phase of rejection (gaping). Studies employing electrical-stimulation induced motor activity have localized interneurons controlling these complex motor patterns to the medullary reticular formation (RF), but the characteristics of these neurons during more naturally induced behavior are unknown. The purpose of the present study was to record the activity profiles of RF neurons during licking, swallowing, and oral rejection in response to gustatory stimulation. Two-hundred and two neurons recorded from awake, freely moving rats were broadly classified as orally related (67%) or non-orally related (33%). Orally related neurons included a large number that were rhythmically active during licking (n = 76; 38%). These "lick-rhythmic" neurons were widely distributed in the RF, but were concentrated in the caudal medullary reticular formation adjacent to the hypoglossal nucleus (Probst's region) and further rostral in the intermediate zone (IRt) of the RF. An analysis of autocorrelations determined that lick-rhythmic neurons in these regions were more closely coupled to licking than to lick-rhythmic neurons more lateral in the parvocellular RF (PCRt). In addition to neurons with weak lick-rhythmic activity, the PCRt also contained a disproportionate number of neurons with orosensory or mixed oro-sensorimotor properties. These data provide evidence for functional specialization within different regions of the medullary RF. A high proportion of lick-rhythmic neurons also showed differential activity associated with swallowing (41%) and/or gaping (75%), further suggesting that the different components of ingestion and rejection share brainstem substrates instead of being produced by unique subsets of interneurons.

Neurotransmitter phenotypes of intermediate zone reticular formation projections to the motor trigeminal and hypoglossal nuclei in the rat

“…Recording from cortically induced rhythmically firing neurons that were either in phase with jaw-opening or jaw-closing, and that projected to the appropriate motor pool in mV, suggested two classes of excitatory premotoneurons in the PCRt (Nozaki et al, 1993). In addition to pre-oromotor projections that respond rhythmically in response to cortical stimulation (Inoue et al, 1994;Sahara et al, 1996;Nozaki et al, 1993), the IRt has neurons rhythmically active during licking, oral rejection, and chewing in the chronic, awake state (Hiraba et al, 1988;Travers et al, 2000) and reversible lesions with muscimol infusions into the combined PCRt/IRt suppressed lingualmasticatory consummatory activity in the awake rat (Chen et al, 2001).…”

Cerebellum and Cerebellar Connections

“…As such it has been suggested to be specifically involved in food manipulation. Indeed, the lateral and intermediate medullary reticular formation of the rat have been demonstrated to contain pre-oromotor neurons (Travers et al, 2000) and are involved with mastication and swallowing (Luo et al, 2001). Additional projections from the IntDL reach the posterior nucleus of the thalamus (Bentivoglio and Molinari, 1986;Teune et al, 2000).…”

Oromotor Nuclei

“…Cortical sites that support microstimulation-elicited ororhythmic responses send projections to widespread regions of the lateral medullary and pontine reticular formation (Zhang and Sasamoto, 1990). These regions in the brainstem overlap the location of neurons that fire rhythmically during licking (Travers et al, 2000) or to cortical microstimulation (Moriyama, 1987) as well as the location of neurons that project to 12N (Travers and Norgren, 1983). Descending projections from limbic structures to the midbrain provide additional pathways through which forebrain structures III.…”