Quantitative analysis of the bilateral brainstem projections from the whisker and forepaw regions in rat primary motor cortex

Abstract

The whisker region in rat primary motor (MI) cortex projects to several brainstem regions, but the relative strength of these projections has not been characterized. We recently quantified the MI projections to bilateral targets in the forebrain , and the present study extends those findings by quantifying the MI projections to bilateral targets in the brainstem. We found that both the whisker and forepaw regions in MI project most strongly to the basal pons and superior colliculus. While the MI forepaw region projects mainly to the ipsilateral basilar pons, the MI whisker region has significantly more connections with the contralateral side. This bilateral difference suggests that corticopontine projections from the MI whisker region may have a role in coordinating bilateral whisker movements. Anterograde tracer injections in MI did not reveal any direct projections to the facial nucleus, but retrograde tracer injections in the facial nucleus revealed some labeled neurons in MI cortex. The number of retrogradely-labeled neurons in MI, however, was dwarfed by a much larger number of labeled neurons in the superior colliculus and other brainstem regions. Together, our anterograde and retrograde tracing results indicate that the superior colliculus provides the most effective route for transmitting information from MI to the facial nucleus. Indexing termsanterograde tracing; corticopontine; corticoreticular; corticotectal; facial nucleus; motor control; retrograde labeling Many rodents, including rats and mice, display repetitive bilateral sweeping movements of the whiskers while exploring their environment (Welker, 1964;Rice, 1995;Gao et al., 2001;Sachdev et al., 2003;Sellien et al., 2005). These rhythmic movements consist of protractions and retractions mediated by three sets of muscles (Hill et al., 2008). Each whisking cycle is initiated by contractions of the rostral-lying musculus nasalis, which pulls the whisker pad forward. Contractions of the intrinsic sling muscles rapidly pivot the whiskers further forward to produce the full extent of whisker protraction. During retraction, the nasalis and sling muscles relax while two caudal-lying muscles, the nasolabialis and maxillolabialis, contract to pull the whisker pad backward. Neuronal tracing and physiological stimulation studies indicate that the lateral facial nucleus contains most of the motoneurons that control these muscles (Klein and Rhoades, 1985;Semba and Egger, 1986;Herfst and Brecht, 2008 NIH-PA Author ManuscriptNIH-PA Author Manuscript NIH-PA Author ManuscriptWhile the kinematics of whisker movements (e.g., amplitude, frequency, whisking phase) vary substantially across different behavioral situations, most whisking behavior is characterized by some degree of bilateral coordination. Exploratory whisking is often marked by epochs (1-2s) of bilaterally-symmetric movements in which whiskers on both sides of the head move synchronously at similar amplitudes and frequencies (Gao et al., 2001;Sachdev et al., 2003;Sellien et al., 2005). During h...

Neuronal Basis for Object Location in the Vibrissa Scanning Sensorimotor System

“…Cerebellar projection cells respond to vibrissa input (Bosman et al, 2010) and cerebellar output can affect the timing in vM1 cortex (Lang et al, 2006), but again there is no composite understanding. The situation is more advanced for the case of the superior colliculus, which receives direct vibrissa input via a trigeminotectal pathway (Killackey and Erzurumlu, 1981; Figure 3), indirect input via a corticotectal pathway through vS1 and vM1 cortices (Alloway et al, 2010; Miyashita et al, 1994; Wise and Jones, 1977) and can drive whisking as well (Hemelt and Keller, 2008). Recording in awake free ranging animals show that cells in the colliculus respond to vibrissa touch (Cohen and Castro-Alamancos, 2010), while experiments that used fictive whisking with anesthetized animals show that cells can respond to movement in the absence of contact (Bezdudnaya and Castro-Alamancos, 2011).…”

Descending projections from the dysgranular zone of rat primary somatosensory cortex processing deep somatic input

“…This suggests that SI processing of deep somatic input may preferentially influence information processing in APT. The APT was also shown to receive input from the MI forepaw and whisker areas (O'Donoghue et al, 1987;Miyashita et al, 1994;Alloway et al, 2010). However, these MI projections terminate more dorsally in APT.…”

“…Descending projections from MI were also shown to terminate in RN (Gwyn and Flumerfelt, 1974;Giuffrida, 1991;Miyashita et al, 1994;Alloway et al, 2010). The RN, through its connections with the cerebellum, inferior olive, and spinal cord (Gwyn, 1971;Murray and Gurule, 1979;Huisman et al, 1983;Swenson and Castro, 1983;Kennedy, 1990), participates in locomotive coordination of the shoulder and upper limbs and also in skilled movement of the forelimbs (Lawrence and Kuypers, 1968;Gibson et al, 1985;Whishaw et al, 1998;Muir and Whishaw, 2000).…”

Oromotor Nuclei

“…Different divisions of 7N receive substantial and differential input, primarily from nuclei of the midbrain, pons, and medulla (Erzurumlu and Killackey, 1979;Hinrichsen and Watson, 1983;Travers and Norgren, 1983;Isokawa-Akesson and Komisaruk, 1987;Mogoseanu et al, 1994;Fay and Norgren, 1997b;Pinganaud et al, 1999;Grinevich et al, 2005;Alloway et al, 2010). A direct projection from the motor cortex to motoneurons innervating the vibrissae is also evident (Grinevich et al, 2005).…”

“…However, studies with more conventional tracers concluded that, quantitatively, the superior colliculus provided the most direct pathway between the vibrassal motor cortex and vibrissae motoneurons (Alloway et al, 2010). The contralateral red nucleus further provides a relay for cortical and cerebellar input to 7N, and electrical stimulation of the red nucleus produced movement of both the vibrissae and eyelid (Hinrichsen and Watson, 1983;Isokawa-Akesson and Komisaruk, 1987;Hattox et al, 2002).…”