The olivo-cerebellar system and its relationship to survival circuits

Abstract

How does the cerebellum, the brain's largest sensorimotor structure, contribute to complex behaviors essential to survival? While we know much about the role of limbic and closely associated brainstem structures in relation to a variety of emotional, sensory, or motivational stimuli, we know very little about how these circuits interact with the cerebellum to generate appropriate patterns of behavioral response. Here we focus on evidence suggesting that the olivo-cerebellar system may link to survival networks via interactions with the midbrain periaqueductal gray, a structure with a well known role in expression of survival responses. As a result of this interaction we argue that, in addition to important roles in motor control, the inferior olive, and related olivo-cortico-nuclear circuits, should be considered part of a larger network of brain structures involved in coordinating survival behavior through the selective relaying of "teaching signals" arising from higher centers associated with emotional behaviors.

Keywords: cerebellum; inferior olive; modules; periaqueductal gray; survival.

FIGURE 1

PAG-olivo-cerebellar connectivity. (A) Microinjection of viral anterograde tracer (AAV-CMV-eGFP) into the vlPAG (left panel, injection site indicated by arrowhead; scale bar, 0.5 mm) leads to terminal labeling in the medial accessory olive (middle panel, indicated by arrowheads; scale bar, 100 μm) and dorsal accessory olive (right panel, indicated by arrowheads; scale bar, 30 μm) and also principal olive (not shown). (B) Left, posterior view of the rat cerebellum illustrating the distribution of responses evoked by stimulation of left dlPAG at intensity of 2x threshold in one experiment under sodium pentobarbital anasthesia (60 mg/kg administered intraperitoneally). Mean peak-to-trough amplitude (three trials) is represented by the size of filled circles. Right, example waveforms (superimposition of eight consecutive responses) obtained from the recording position indicated on the cerebellar schematic. Stimulus delivered at start of each trace. Scale bar, 15 ms and 0.2 mV. (C) Example of four consecutive responses recorded from the same position on the cerebellar cortex. Filled arrow heads indicate timing of PAG stimulation. Scale bars, 20 ms and 0.2 mV. Reproduced with permission from Flavell (2008) and Crook et al., unpublished.

FIGURE 2

The PAG can modulate SOCPs supraspinally. Climbing fiber fields evoked by stimulation of contralateral hindlimb (H/Limb), ipsilateral dorsal funiculus (DF) and contralateral ventral funiculus (VF) are all significantly suppressed following microinjection of an excitatory amino acid (D-homocysteic acid, DLH) into the vlPAG. Stimulation onset indicated by filled arrowheads. Each trace is an average of 15 trials. Each bar is the mean + SEM of n = 15 trials. *P < 0.05; **P < 0.01. Scale bar values are the same for each trace. Reproduced with permission from Cerminara et al. (2009).