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Brainstem Control of Head Movements During Orienting; Organization of The Progress in Neurobiology 66 (2002) 205–241 Brainstem control of head movements during orienting; organization of the premotor circuits Tadashi Isa a,∗, Shigeto Sasaki b a Department of Integrative Physiology, National Institute for Physiological Sciences, Myodaiji, Okazaki 444-8585, Japan b Department of Neurophysiology, Tokyo Metropolitan Institute for Neuroscience, Musashidai, Fuchu 183-8526, Japan Received 26 July 2001; accepted 10 December 2001 Abstract When an object appears in the visual field, animals orient their head, eyes, and body toward it in a well-coordinated manner (orienting movement). The head movement is a major portion of the orienting movement. Interest in the neural control of head movements in the monkey and human have increased in the 1990’s, however, fundamental knowledge about the neural circuits controlling the orienting head movement continues to be based on a large number of experimental studies performed in the cat. Thus, it is crucial now to summarize information that has been clarified in the cat for further advancement in understanding the neural control of head movements in different animal species. The superior colliculus (SC) has been identified as the primary brainstem center controlling the orienting. Its output signal is transmitted to neck motoneurons via two major separate pathways: one through the reticulospinal neurons (RSNs) in the pons and medulla and the other through neurons in Forel’s field H (FFH) in the mesodiencephalic junction. The tecto-reticulo-spinal pathway controls orienting chiefly in the horizontal direction, while the tecto-FFH-spinal pathway controls orienting in the vertical direction. In each pathway, a subgroup of neurons functions as premotor neurons for both extraocular and neck motoneurons, while others are specified for each, which allows both coordinated and separate control of eye and head movements. Head movements almost always produce shifts in the center of gravity that might cause postural disturbances. The postural equilibrium may be maintained by transmitting the orienting command to the limb segments via descending axons of the reticulospinal and long propriospinal neurons. The SC and brainstem relay neurons receive descending inputs from higher order structures such as the cerebral cortex, cerebellum, and basal ganglia. These inputs may serve context-dependent control of orienting by modulating the activities of the primary brainstem pathways. © 2002 Elsevier Science Ltd. All rights reserved. Contents 1. Introduction ............................................................................... 206 2. Behavioral analysis of head movements during orienting ...................................... 207 2.1. A common organization in the head motor system and biomechanical constraint ............ 207 2.2. General characteristics of orienting in unrestrained cats ................................... 208 2.3. Visually guided orienting to moving versus stationary stimuli ............................. 208 3. Primary brainstem pathways controlling orienting ............................................ 209 3.1. Superior colliculus (SC); brainstem center of orienting ................................... 210 3.1.1. Microstimulation of the SC......................................................... 210 Abbreviations: BC, m. biventer cervicis; BCC, m. biventer cervicis and complexus; C-RSNs, “cervical” reticulospinal neurons; CTT, central tegmental tract; CP, cerebral peduncle; CUN, cuneiform nucleus; EPSP, excitatory postsynaptic potential; FEF, frontal eye field; FFH, Forel’s field H; FR, fasciculus retroflexus; FN, fastigial nucleus; G, genu of facial nerve; HRP, horseradish peroxidase; INC, interstitial nucleus of Cajal; IO, inferior olive; LED, light emitting diode; LGN, lateral geniculate nucleus; L-RSNs, “lumbar” reticulospinal neurons; MLF, medial longitudinal fasciculus; MNs, motoneurons; NR, nucleus ruber (red nucleus); NRGc, nucleus reticularis gigantocellularis; NRPc, nucleus reticularis pontis caudalis; PAG, periaqueductal grey matter; PH, prepositus hypoglossi; PNs, phasic neurons; PSNs, phasic sustained neurons; Pyr, pyramidal tract; Rp, raphe region; RSN, reticulospinal neuron; SC, superior colliculus; SCUN, subcuneiform nucleus; SGI, stratum griseum intermediale (intermediate layer of SC); SGP, stratum griseum profundum (deep layer of SC); SGS, stratum griseum superficiale (superficial layer of SC); SN, substantia nigra; SNr, substantia nigra pars reticulata; SPL, m. splenius; TB, trapezoid body; Tec, tectum; TNs, tonic neurons; TR(S)N, tectoreticular and tectoreticulospinal neuron; VN, vestibular nucleus; III, oculomotor nucleus; VI, abducens nucleus; VII, facial nucleus ∗Corresponding author. Tel.: +81-564-55-7859; fax: +81-564-55-7790. E-mail address: [email protected] (T. Isa). 0301-0082/02/$ – see front matter © 2002 Elsevier Science Ltd. All rights reserved. PII: S0301-0082(02)00006-0 206 T. Isa, S. Sasaki / Progress in Neurobiology 66 (2002) 205–241 3.1.2. Lesion studies of the SC ........................................................... 210 3.1.3. Single unit recordings in the SC .................................................... 212 3.1.4. Descending and ascending projections from the SC................................... 212 3.2. Brainstem relay of the descending commands from the superior colliculus to neck motoneurons 213 3.2.1. Tectoreticulospinal pathways via the pontomedullary reticular formation ............... 213 3.2.2. Tectoreticulospinal pathways via the reticular formation in the mesodiencephalic junction 217 4. Effects of lesion of the brainstem relay structures on orienting head movements ................ 220 4.1. The pontomedullary reticular formation ................................................. 220 4.2. Forel’s field H......................................................................... 221 5. Single unit activities of neurons in the brainstem reticular formation during orienting............ 221 5.1. Single unit activity of neurons in the pontomedullary reticular formation ................... 221 5.1.1. Directional tuning of the NRPc and NRGc neurons during orienting ................... 221 5.1.2. Firing pattern of reticular neurons and their morphological and physiological correlates . 223 5.2. Single unit activity of neurons in Forel’s field H ......................................... 225 6. Differential control of horizontal and vertical components of head movements .................. 226 7. Higher order structures that regulate the primary brainstem pathways for orienting .............. 228 7.1. Pericruciate cortical areas .............................................................. 228 7.2. Cerebellum ........................................................................... 232 7.2.1. Effects of functional inactivation .................................................... 232 7.2.2. Efferent projection from the fastigial nucleus ........................................ 233 7.3. Basal ganglia ......................................................................... 233 7.3.1. Effects of electrical stimulation ..................................................... 233 7.3.2. Descending projection from the basal ganglia ........................................ 233 7.3.3. Role of basal ganglia in control of orienting triggered by volitional intention ........... 233 8. Posture adjustment during orienting head movements ......................................... 233 9. Other animal species ....................................................................... 234 9.1. Primates .............................................................................. 234 9.1.1. Role of the SC in orienting head movements in primates ............................. 235 9.1.2. Descending pathway from the SC in primates........................................ 235 9.1.3. Involvement of the FEF in orienting head movements in primates ..................... 235 9.2. Rodents .............................................................................. 235 9.3. Barn owl ............................................................................. 236 10. Conclusion ............................................................................... 236 References ................................................................................... 237 1. Introduction eye movements in the head-restrained condition. Stud- ies on the neural control of orienting movements in Orienting is defined as the gaze shift from one point an unrestrained condition have been done mainly in to another in space that animals make to fixate an object. cats except for early studies by Bizzi and colleagues in Orienting is observed in a wide variety of animals. Thus, primates (Bizzi et al., 1971, 1972a,b; Dichgans et al., the basic component of the neuronal pathways controlling 1973; Bizzi, 1979). Neural mechanisms for control of head orienting is presumed to be common over animal species. movements in primates have received much attention since The orienting movements are comprised of coordination of 1990. However, because of the lack of detailed knowledge different body parts such as the eyes, head, and trunk. The about the neuronal pathways controlling the orienting head body architecture differs among the animal species, which movements, interpretation of the behavioral data obtained may lead to addition of adaptive circuits to the primary com- in monkeys should largely rely on the knowledge accumu- ponent of the circuit. For instance, the oculomotor range, lated from
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