Much like the telencephalon, which eventually evolved into the neocortex of mammals, the cerebellum too has existed in vertebrates for hundreds of millions of years evolving in parallel with the telencephalon (Cisek 2019). At least in mammals, the ratio of telencephalic (i.e., neocortical) neurons to cerebellar neurons is preserved at about 1 to 4 from rodents to primates (Herculano-Houzel 2009, 2010, 2012). This suggests a structural co-evolution between the telencephalon and cerebellum, since it is believed that small mammals existed before the extinction of dinosaurs (65 mya) and primate diversification followed this extinction (Zhang et al. 2008). Whereas the telencephalon can be thought of as a hub for sensory integration and information storage (Zacks and Jablonka 2023), the cerebellum is dedicated to motor control, as suggested (Eccles 1967) and now to be argued.

Just how is the cerebellum related to consciousness? In humans, the neocortex becomes active well in advance of one’s conscious awareness to move in the form of a readiness potential (recorded from the frontal lobes), once one is overtrained on a behavior (Libet 1985; Soon et al. 2008). The source of this neocortical discharge comes from the cerebellum, since damage of the output fibres from the cerebellum abolishes the readiness potential (Ikeda et al. 1994). The relationship between the neocortex and cerebellum has now been assessed in detail using behaving mice, optogenetics, and silicon probe recording. This has been done by studying all the major pathways between the neocortex and the cerebellum by Hasanbegović and her colleagues (Gao, De Zeeuw et al. 2018; Hasanbegović 2024; Hasanbegović et al. 2023; Zhu, Hasanbegović 2022). The pathways, which exist in all mammals including rodents and primates, are summarized in Figure 1.

To study the neocortical-cerebellar loop, head-fixed mice were trained on a tactile memory task that entailed responding to a manipulandum that contacted a front or back location of the whiskers on the right side of the body, for example (typically on the side contralateral to the neocortical area under study, Hasanbegović 2024). Afterwards, the mouse was required to remain quiet for a 1 second delay period. At the end of the delay period, an auditory tone was delivered, which signaled the mouse to lick either a left or right spout to obtain a liquid reward. If the front whisker was contacted the mouse had to lick the left spout, and if the back whisker was contacted the mouse had to lick the right spout. Once trained, a mouse could hold the position of a touch in memory to lick at a percent-correctness rate of 80% or better (chance was 50% correctness).

Two important observations were made of the activity and functional necessity of the neurons at each junction comprising the loop (Gao, De Zeeuw et al. 2018; Hasanbegović 2024; Hasanbegović et al. 2023; Zhu, Hasanbegović 2022). First, during the memory period neurons were found throughout the loop—i.e., in the neocortex (the anterolateral motor cortex), the pons, the cerebellum, and the thalamus—that discharged during this period anticipating the correct response. Second, when optogenetics was used to silence the neurons throughout the loop during the memory period, the choice behavior of an animal was compromised (but licking behavior was not). Thus, for the execution of the tactile memory task, all parts of the neocortical-cerebellar loop are operative and necessary. This finding agrees with the observation that the readiness potential is abolished in humans, after disrupting the neocortical-cerebellar loop at the level of the cerebellum.

Given the dependency of the neocortex on the cerebellum, great effort has gone into mapping the topographic correspondence between the neocortex and the cerebellar cortex in humans using resting-state functional-connectivity MRI (Buckner 2013; Buckner et al. 2011; Diedrichsen et al. 2019; Marek et al. 2018). Before describing these results, it is important to have a clear picture of how the human cerebellar cortex is configured anatomically showing that it is divided into three major regions, the anterior lobe, the mediolateral lobe, and the posterior lobe (see Figure 2). It was discovered that there is a systematic correspondence between the cortex of the neocortex and the cortex of the cerebellum, such that sensorimotor regions of neocortex (areas M1 and S1,S2, & S3) are connected to the anterior lobe, the object encoding regions (the extrastriate, the temporal, and the orbital cortices) are connected to the mediolateral lobe, and the motion encoding regions (the medial temporal, the superior medial temporal, the superior temporal sulcus, the posterior parietal, and the supplementary motor cortices) are connected to the posterior lobe. Also, the posterior vermis including the flocculonodular lobe is connected to cingulate regions that mediate interoception.

Even though the forgoing connectivity scheme has been used to suggest that the cerebellum mediates cognition (Van Overwalle et al. 2023; Xue, Buckner et al. 2021; see Footnote 1), this conclusion is based on a misthinking of sensorimotor neurophysiology. First, the cerebellum operates according to a motor, spike-rate code (rather than a sensory, receptive-field code, which is characteristic of the neocortex) (Schiller and Tehovnik 2015; Tehovnik et al. 2021). In primates (e.g., macaque monkeys), the cerebellum utilizes a spike-rate code when transmitting signals to the cerebellar nuclei, which are the output neurons that innervate the eye movement generator in the brain stem, as well as circuits that regulate head and body movements (Kheradmand and Zee 1991; Manto et al. 2012). By increasing the frequency of pulses or length of the train duration, the size of saccadic eye movements evoked electrically from the cerebellar vermis (lobules VI and VII) increases (Noda and Fujikado 1987b). Moreover, the discharge duration of cerebellar neurons defines the size of a saccadic eye movement such that the longer the duration, the greater the displacement (Fuchs et al. 1993; Ohtsuka and Noda 1991). Furthermore, current pulses as low as 2-3 μA delivered in 20 ms trains are sufficient for evoking saccades from the cerebellum (Noda and Fujikado 1987a). By comparison, current pulses higher than 10 μA and at much longer train durations (i.e., from 50 to 200 ms) are needed to generate ocular responses from the neocortex (Schiller and Tehovnik 2015; Tehovnik and Slocum 2004; Tehovnik and Sommer 1997). A major reason for this difference is that Purkinje cells respond well to high-frequency stimulation (i.e., optimally at 600 Hz, Noda and Fujikado 1987b), which attests to the extreme excitability of their axon initial segments (Foust et al. 2010). Finally, if electrical stimulation is introduced to the cerebellum during an ongoing saccadic eye movement, the movement is interrupted instantly, and a new saccade is generated as encoded by the site of stimulation (Noda and Fujikado 1987a; Noda et al. 1991). A similar result occurs for stimulation of the eye movement generator (Cohen and Komatsuzuki 1972). Accordingly, the cerebellum has priority access to the eye movement generator in the brain stem for saccade execution. This is not true of the neocortex. Electrically evoked ocular responses elicited from the neocortex can readily be interrupted by an animal’s ongoing behavior (Chen and Tehovnik 2007; Tehovnik and Slocum 2004). Thus, the cerebellum’s oculomotor control is predicated on having direct access to the movement controllers by way of a spike-rate code. This permits for the execution of effortless body movements as triggered by a specific sensory context, once a task has been learned or contemplated (Hebb 1949, 1968; Swain et al. 2011; Thach et al. 1992).

Second, in humans born without a cerebellum, all motor functions are impaired while consciousness is still present (see Footnote 2, Yu et al. 2014). For example, word generation loses its spontaneity, speed, and rhythmicity in the absence of the cerebellum. Indeed, by eliminating the cerebellum or by cutting the connections between the neocortex and the cerebellum, consciousness becomes rudderless (rather than absent), in that the body can no longer be controlled by the neocortex. As already understood, disconnecting the neocortex from subcortical networks by destruction of the pons and thalamic nuclei initially induces coma (Plum and Posner 1980), and if-and-when there is recovery it is based on the order of recovery of the specific modules between the neocortex and cerebellum. For example, if there is damage to circuits mediating language in a polylingual individual, the primary language is restored first followed by the secondary languages (Mariën et al. 2017), and this follows from different languages being controlled by independent neocortical-cerebellar networks (Mariën et al. 2017; Ojemann 1991, 1983). Also, cerebellar damage does not eliminate body movement, but mainly affects proprioceptive and vestibular functions (Miles and Lisberger 1981; Ioffe 2013; Fuchs and Kornhuber 1969; see Footnote 3), which is non-trivial since such damage can produce a state where a patient continues to right him or herself even when he or she is gravitationally level.

Third, the cerebellum is organized into relatively independent modules, whereas the neocortex is highly interconnected (Tononi 2008)—with overlapped modules (or streams of consciousness, James 1890)—for the maximal exchange of information during learning and conscious reflection (Hebb 1949, 1968). The cerebellar modules are organized according to the myotomes of the body (Thach et al. 1992), whereby distinct sectors are dedicated to distinct body parts (see Footnote 4). Like a puppeteer, the neocortex innervates the cerebellar modules according to need (Hasanbegović 2024). The connectivity profile of Bolt, Pelé, Kasparov, and Einstein would be very different, since each had dedicated a lifetime of effort to enhancing the unique communications between their consciousness and their motor system from running down a track, to moving a ball on a pitch, to sliding pieces on a chess board, to imagining principles of physics which eventually needed to be put on paper using mathematical notation.

Summary:

1. The cerebellum and neocortex evolved in parallel, and in rodents and primates the number of neurons is set at a ratio of 4 to 1.

2. The functionality of the cerebellum and neocortex are highly dependent, and pathways link the two by way of a functional loop; to study the cerebellum in the absence of the neocortex (or vice-versa) will lead to an incomplete understanding of consciousness.

3. The cerebellum operates according to a motor, spike-rate code, and the neocortex operates according to a sensory, receptive-field code.

4. The absence or damage of the cerebellum does not eliminate consciousness, but rather it interrupts the expression of consciousness through well-composed motor responses.

5. The cerebellum is organized according to myotomes, each of which is responsible for the movement of a specific body part; the neocortex, on the other hand, is well-integrated synaptically, which permits rapid learning and consciousness.

Footnote 1: Which is according to the surmise of Schmahmann (1997).

Footnote 2: Even though consciousness is severely retarded because the motor outputs have been compromised because of proprioceptive and vestibular problems.

Footnote 3: Also, locomotion is not abolished if the neocortex is ablated (Vanderwolf 2007; Vanderwolf et al. 1978).

Footnote 4: Myotomes are a group of muscle fibres innervated by a single spinal nerve composed of sensory and motor roots. They are represented mainly coronally in the cerebellar cortex and thus project parallel to the trajectory of the parallel fibers of the cerebellum, the fibres that originate from the most numerous neurons, i.e., the granular cells, in the brains of all mammals (Herculano-Houzel 2009). The parallel fibres project along the length of a lobule, and they are situated orthogonal to the climbing fibres (from the inferior olive) of the cerebellum. It is the climbing fibres (one per Purkinje neuron) that adjust the gain of the Purkinje neurons, which are central to efference-copy encoding. Since the parallel fibres are connected to the nuclear cells via Purkinje neurons, a beam of parallel fibres in combination with the climbing fibres control the modulation of the nuclear neurons (in the fastigial, interpositus, and dentate nuclei) to affect the synergistic activation of the muscles of a myotome, thereby controlling all multijointed movements in mammals including humans.

Figure 1: The neocortical-cerebellar loop. Regions of the neocortex (Neocortex) connect to the cerebellum by way of the pontine nuclei (Pons). At the pontine nuclei, the fibres cross the midline to occupy the middle cerebellar peduncle forming the mossy fibres that innervate the granular neurons (the most numerous neurons in the mammalian brain, not shown), which then connect to the Purkinje neurons (Purkinje neurons) by way of the parallel fibres. The Purkinje neurons are the output fibres of the cerebellar cortex and they innervate the cerebellar nuclei (Cerebellar nuclei, of which there are three going from the midline to lateral, respectively: fastigial, interpositus, and dentate), which send projections to the thalamus (Thalamus, as well as the brain stem and spinal cord movement generators). The thalamus innervates the neocortex, completing the loop. The increased firing of the Purkinje neurons decreases the neural firing within the cerebellar nuclei, and the decreased firing of the Purkinje neurons increases the firing within the cerebellar nuclei. This see-saw arrangement is regulated by the climbing fibres from the inferior olive (not shown) to optimize motor performance through training.

Figure 2: Schematic of a top view of the human cerebellum divided into three lobes: anterior, mediolateral, and posterior. According to the fMRI experiments of Boillat et al. (2020), who used a 7-tesla scanner, a somatotopy—for the eye, the tongue, the hand and the foot—is found for the anterior and posterior lobes, but an eye representation without a clear somatotopy is found for the mediolateral lobe. A head representation is found in lobule VI (Manni and Petrosini 2004), and vestibular control of the head is found in lobule X (Lisberger and Fuchs 1978). The text inset in the upper left defines the movement of the body part or sense that triggered a maximal response within the cerebellar cortex.