One of the first studies to deduce how structures external to the cerebellum are involved in setting the adaptation signal in the cerebellum during learning has been performed by Soetedjo, Fuchs and colleagues (2019). Monkeys were trained to generate a saccadic eye movement to a punctate visual target such that during the execution of a saccade the target was stepped toward or away from the starting point of the saccade. When subjected to such conditions repeatedly for one direction of target shift, monkeys learn to anticipate the direction of the shift by altering the amplitude of the saccadic eye movement. Prior to learning, a monkey produced a corrective saccade to acquire the target. It is the change in complex spikes by way of the inferior olive that alters the Purkinje cell firing rate in the cerebellum in that decreases in saccade amplitude are accompanied by a reduction of simple spikes and increases in saccade amplitude are accompanied by an addition of simple spikes. The adaptation signal via the complex spikes can be manipulated by electrically stimulating or by chemically inactivating populations of cells in the superior colliculus that encode saccade metrics (Soetedjo et al. 2019). Once adaptation is finalized, however, such manipulations are ineffective (much like what happens for the learning of the eyeblink conditioning response, Swain, Thompson et al. 2011). The superior colliculus contains a topographic map for the generation of visually-guided saccadic eye movements (Schiller and Tehovnik 2015); therefore, it sends a ‘where’ signal to the inferior olive so that a visual object is acquired efficiently and any change in the sensorimotor circumstances produces a change at the cerebellar Purkinje cell synapses, so that the eyes arrive on target via the climbing fibre adaptation channel. This is the ‘where’ component of the response (see Fig. 1, circuits colored in purple).
Unlike the superior colliculus, which codes for where a visual object is located, the neocortex contains cells that code for the ‘what’ aspects of an object such as its luminance, color, shape, depth, motion, and so on (Schiller and Tehovnik 2015). The temporal lobes are known to house neurons that fire to a specific collection of features of an object and damage to this part of the brain impairs object recognition in monkeys and humans (as does damage to the medial temporal cortex impair objects defined by motion). Based on the observations of Soetedjo, Fuchs and colleagues (2019), if one were required to generate an eye movement to a new object such as the letter B after having learned to make such a response to letter A, two things need to happen: (1) the firing of cells in the temporal cortex should shift from those coding for object A to those coding for object B (which are induced by changes in reward contingency); (2) during the transition period from object A to B the inferior olive alters the synaptic configuration at the cerebellar Purkinje cells mediating the response such that object B is made to evoke the response that was once evoked by object A, as signaled to the Purkinje neurons by altering the composition of mossy fibres activated (Marr 1969) (see Fig. 1). Once the new configuration is complete (with optimal performance in terms of percent-correctness at the shortest latency) the inferior olive is disengaged from the cerebellum. Object B has now replaced object A for generating the response, fictively from the cerebellum (for the cerebellum is an efference copy decoder) that receives the same information as the saccade generator for response execution. The foregoing process applies universally to any type of body movement since the cerebellum is privy to all skeletomotor responses subserved by the skeletal muscles.
Figure 1: The neocortex of primates mediates the ‘what’ characteristics of a visual target and the superior colliculus mediates the ‘where’ or location characteristics of a visual target. Symbols ‘A’ and ‘B’ are stored in the temporal cortex declaratively after learning. To communicate the ‘what’ and ‘where’ properties of the symbols to the cerebellum, the mossy fibres carry the pattern of the symbols to the cerebellar cortex (Marr 1969) and the climbing fibres carry the location signal to the cerebellar cortex (Soetedjo, Fuchs and colleagues 2019). The two signals are merged during learning so that once associated a saccadic eye movement is generated to a symbol at the appropriate time, i.e., ‘when’. To drive the saccadic behavior, i.e., the ‘why’, a reward signal is transmitted from the ventral tegmental area (VTA) to the cerebellar cortex via the climbing fibres. Other labels are as follows: visual cortex (V1), motor cortex (M1), and superior colliculus (SC).