Behavioral organization of reticular formation: studies in the unrestrained cat. I. Cells related to axial, limb, eye, and other movements

Abstract

1. We have recorded single-unit activity in medial reticular formation (RF) units in unrestrained, behaving cats. A total of 306 cells have been analyzed. Neuronal activity was observed during a variety of natural, spontaneously occurring behaviors, during rapid eye movement (REM) and non-REM sleep states, after sensory stimulation, and during elicited reflexes.

2. Most RF units discharged maximally in conjunction with a specific movement or group of movements. The companion paper (41) deals with cells related to movements of the facial musculature, while the present paper deals with all other cell types.

3. The most common RF cell types discharged during specific movements of the axial skeleton. Cells related to limb, respiratory, pharyngeal and laryngeal, jaw, and tongue movements were also observed. Reticular eye movement-related cells, previously investigated by others, were also seen in our unrestrained cats. A small percentage of cells were maximally activated by applied auditory, visual, vestibular, somatosensory, or proprioceptive stimuli.

4. Cells related to axial movement, which as a group constituted 38.2% of all RF cells, could be subdivided into cells related to neck extension, neck dorsiflexion, and ipsilateral or contralateral movement of the spine.

5. Cells related to active ipsilateral movement, constituting 19.3% of all medial RF cells, were the single most common cell type in the RF. Thirty-four percent of these cells did not respond to passive head movement, while 48% responded to passive head movement to the contralateral side and 18% to passive movement to the ipsilateral side. Neck proprioceptors contribute to the passive movement response in certain of these cells.

6. Cells related to limb movement constituted 6.9% of the cells encountered. Most were related to movement of the proximal portion of one limb. Cells related to movement of the distal portion of the limb were quite rare, constituting only 1.0% of RF cells.

7. While most RF cells were active only in relation to a single, directionally specific movement, we found a cluster of pontine RF cells, which discharged in relation to several limb and neck movements.

8. Cells related to several movements, eye movement, vestibular stimulation, and cells without spontaneous activity in sleep or waking were localized to restricted portions of the medial RF fields. Cells related to axial, proximal limb movements or somatic stimulation were intermingled throughout the entire region explored.

9. The unrestrained preparation allows the direct observation of the behavioral correlates of increased RF unit discharge. Most RF cells discharge in relation to a specific movement or group of movements of the axial musculature. Each movement-defined cell type has a different pattern of sleep, sensory and reflex activity, and anatomical localization. Anatomical intermingling of certain cell types may facilitate the synthesis of complex movement sequences from simpler elements commanded by individual RF cells.

FIG. 1.

Polygraph recording of splenius EMG and unit activity in three simultaneously recorded RF units. Pen deflections are pulses triggered by window discriminators monitoring unit signals.

FIG. 2.

Locations of all recording points. Between one and five units were recorded at each point. Circles, recording points between 0.5 and 1.4 mm from midline; triangles, recording points between 1.4 and 2.1 mm from midline; crosses, recording points between 2.1 and 2.5 mm from midline. Abbreviations: FTG, FTM, FTC, gigantocellular, magnocellular, and central tegmental fields; IO, inferior olive; TB, trapezoid body; TR, tegmental reticular nucleus; PG, pontine gray.

FIG. 3.

Anatomical distribution of sleep types. Triangles, type 1; squares, type 2; circles, type 3.

FIG. 4.

Location of eye movement cell types. Circles, cells related to ipsilateral eye movement; triangles, cells related to contralateral eye movement; squares, cells related to ventral eye movement.

FIG. 5.

Location of cells related to extension.

FIG. 6.

Location of cells related to dorsiflexion. The most dorsally located dorsiflexion cell, found at Al, C2.3, H+2.0, is not plotted.

FIG. 7.

Location of cells related to active ipsilateral movement. Cells are subdivided into those responding to passive contralateral movement (circles), passive ipsilateral movement (triangles), and those with no response to passive movement (open diamonds).

FIG. 8.

Location of cells related to active contralateral movement.

FIG. 9.

Response of limb movement-related cell to electric pulse stimulation of left proximal scapula (right) and right proximal pelvis (left).

FIG. 10.

Location of cells related to active limb movement. Cells are subdivided into those discharging during movements of the ipsilateral forelimb (filled circles), contralateral forelimb (open circles), ipsilateral hindlimb (filled square), contralateral hindlimb (open squares), or both ipsilateral limbs (filled triangle).

FIG. 11.

Location of cells related to multiple forelimb and neck movements.

FIG. 12.

Location of cells related to vestibular stimulation. Cells related to ipsilateral head acceleration are indicated with circles, while cells related to contralateral acceleration are indicated with squares.

FIG. 13.

Location of cells related to somatosensory stimulation. Cells with unilateral or laterally asymmetrical fields are indicated with circles, while cells with bilaterally symmetrical receptive fields are indicated with squares.