Sinnamon, H. M. - Mesencephalic Locomotor Region

The Structure of Concern Project compares many theoretical models from many disciplines to the Adizes PAEI model, arguing that they must all be reflecting the same underlying phenomenon. One concern structure model is described below.

Several areas of the brainstem produce locomotive behavior when stimulated, and they appear to do so in different behavioral contexts (Jordan, 1998). H. M. Sinnamon has proposed that these locomotor areas be classified into three functional groups: exploratory, appetitive and defensive (Sinnamon, 1993). The idea has been contested (Allen et al, 1996), but Jordan reviews evidence from brain stimulation studies, lesion studies and immunohistochemical studies supporting the mesencephalic locomotor region (MLR) construct.

Locomotive behavioral routines are the product of central pattern generators controlled by descending brainstem reticulospinal pathways. The reticulospinal area receives inputs from the exploratory, appetitive and defensive locomotor systems through the MLR. Activity in the cerebellar fastigial nucleus may also induce locomotion through a relay in the reticulospinal area. Appetitive and defensive input to the MLR comes from the lateral hypothalamus and medial hypothalamus/PAG, respectively. These two hypothalamic sources also send collateral inputs directly to the reticulospinal locomotor area. The exploratory system is driven by inhibitory pallidal output from the basal ganglia that is thought to disinhibit the MLR. Pallidal output does not reach the reticulospinal area directly. (Jordan, 1998)

According to Sinnamon, the role of locomotion differs in these three motivational systems. Primary appetitive locomotion brings the organism in contact with incentive and consummative stimuli. Defensive locomotion places distance between the organism and threatening or painful stimuli. Exploratory locomotion is directed towards distal stimuli in the larger environment. These three locomotor concerns are related to three regions of the MLR as described below in PAEI order:

P – The Primary Appetitive System
Sinnamon maintains that the appetitive and defensive locomotor systems cannot be distinguished in the preoptic basal forebrain. The appetitive system differentiates in the hypothalamus as the perifornical/lateral hypothalamic locomotor region and its downstream targets. This includes direct input to the reticulospinal locomotor area. However, activity in an MLR area called the anterior dorsal tegmentum (ADT) of the midbrain seems necessary for the onset of locomotion evoked by lateral hypothalamic stimulation. GABA injection into this area reversibly blocked lateral hypothalamus-evoked locomotion. Also involved is the deep mesencephalic nucleus and related nuclei.

A – The Primary Defensive System
The defensive behavior network involves the medial hypothalamus and central gray. Under the MLR construct, this system must be further expanded to include the cuneiform region of the midbrain. Electrical and chemical stimulation in all three of these areas gives rise to escape behavior. Labeling studies reveal connections between these and other known elements of the defense system throughout the limbic system, diencephalon, midbrain and hindbrain.

E – The Primary Exploratory System
In the mesencephalon, exploratory locomotion is mediated by the pedunculopontine nucleus. However, it receives input from subpallidal circuits involving hippocampal projections to the accumbens, accumbens projections to the subpallidum, and further projections to and through the zona incerta.

All of these behavior systems are instrumental rather than social, but a ready model for what “social locomotion” might look like is provided by Porges’ Polyvagal theory (Porges, 2003). That theory identifies three components of the autonomic nervous system each associated with a different behavioral strategy. The first and phylogenetically oldest component is the unmyelinated, visceral vagus that slows metabolism and produces immobilization. This can be for digestive purposes or for freezing and playing dead (passive avoidance of threat). The second component is the sympathetic/adrenal system that raises metabolism and inhibits the visceral vagus. It mobilizes ‘fight or flight’ responses to threat. The third and most recently evolved component, unique to mammals, is the myelinated vagus. The regulatory system served by the myelinated vagus can rapidly alternate regulatory effects, shifting between mobilizing and immobilizing the animal, fostering both engagement and disengagement with the environment.

Porges (2001) calls this the “social engagement system”. This kind of cautious, autonomically sensitive stop-and-go locomotion is necessary for social approach in mammalian societies. Porges notes further that the mammalian vagus is structurally and functionally connected to cranial nerves that regulate facial expression and vocalization. These are obviously crucial for social engagement.

The Polyvagal theory stresses the regulatory, sensory and expressive functions of the cranial nerves. Locomotion is not a focal issue for the theory. However, if a social locomotive function were to be defined, some analogue or effect of this social engagement system’s “vagal brake” might prove important.

1. Sinnamon, H. M. (1993). “Preoptic And Hypothalamic Neurons And The Initiation Of Locomotion In The Anesthetized Rat.” Progress in Neurobiology, 41(323-344).
2. Allen, L. F., Inglis, W. L., & Winn, R. (1996). “Is The Cuneiform Nucleus A Critical Component Of The Mesencephalic Locomotor Region? An Examination Of The Effects Of Excitotoxic Lesions Of The Cuneiform Nucleus On Spontaneous and nucleus accumbens induced locomotion.” Brain Research Bulletin 41, (4), 201-210.
3. Jordan, L. M. (1998). “Initiation Of Locomotion In Mammals.” Annals Of The New York Academy of Sciences, 860, 83-93.
4. Porges, S. W. (2001). “The polyvagal theory: phylogenetic substrates of a social nervous system.” International Journal of Psychophysiology, 42, 123-146.
5. Porges, S. W. (2003). “The Polyvagal Theory: phylogenetic contributions to social behavior.” Physiology & Behavior, 79, 503-513.
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