The cerebellar role in perception is predicated on the fact that it is an essential node in the distributed neural circuits subserving sensorimotor, autonomic, and cognitive function as well as emotional processing. The following is a summary of these pathways and connections. For earlier comprehensive reviews and original citations, please see Schmahmann [1–3] and Schmahmann and Pandya [4].

Peripheral Afferents

Auditory and visual inputs are conveyed from primary sensory receptors to vermal lobules VI and VII [5], and visual inputs also reach the dorsal paraflocculus. Spinocerebellar tracts terminate in the sensorimotor cerebellum in the anterior lobe and lobule VIII [6], while vestibular afferents target lobule X [7]. Climbing fibers from the sensorimotor-recipient inferior olivary nuclei project to the sensorimotor cerebellum; the principal olivary nucleus is devoid of peripheral inputs and is linked with the cognitive cerebellum in the posterior lobe (see [3]).

Cerebrocerebellar Pathways

Cerebellar connections with the cerebral cortex include two-stage feedforward and feedback loops with obligatory synapses in the pons and thalamus. The top-down circuit is corticopontine–pontocerebellar and the bottom-up is cerebellothalamic–thalamocortical.

Corticopontine Projections

Knowledge of the corticopontine projections provides critical insights into the nature of the information to which the cerebellum has access. Projections arise from neurons in layer Vb of sensorimotor regions in the precentral, premotor, and supplementary motor area, primary somatosensory cortices, and the rostral parietal lobe [8–11]. Studies in stroke patients also show topography of motor function in the human pons [12].

Considerable corticopontine projections are derived also from the prefrontal cortex, multimodal regions of the posterior parietal and temporal lobes, paralimbic cortices in the cingulate and posterior parahippocampal gyrus, and visual association cortices in the parastriate region, supporting multimodal, supramodal, and limbic related functions necessary for perception (Fig. 1).

Fig. 1 Composite color-coded summary diagram illustrating the distribution within the basis pontis of rhesus monkey of projections derived from association and paralimbic cortices in the prefrontal (purple), posterior parietal (blue), superior temporal (red), parastriate, and parahippocampal regions (orange), and from motor, premotor and supplementary motor areas (green). a Medial, lateral, and orbital views of the cerebral hemisphere from which the projections are derived. b Plane of section through the pons from which the rostrocaudal levels of the pons I through IX are taken. c Patterns of termination within the nuclei of the basis pontis. Other cerebral areas known to project to the pons are depicted in white. Cortical areas with no pontine projections are shown in yellow (from anterograde and retrograde studies) or gray (from retrograde studies). Dashed lines in the hemisphere diagrams represent sulcal cortices. Dashed lines in the pons diagrams represent pontine nuclei; solid lines depict corticofugal fibers (from [1] and [13]) Full size image

Prefrontopontine projections arise from dorsolateral and dorsomedial convexities concerned with attention and conjugate eye movements (area 8), spatial attributes of memory and working memory (area 9/46d), planning, foresight, and judgment (area 10), motivational behavior and decision-making capabilities (areas 9 and 32), and from areas 44 and 45 homologous to language areas in human [13].

Posterior parietal association cortices are critical for directed attention, visual–spatial analysis, and vigilance in the contralateral hemispace; lesions are associated with complex behavioral manifestations. The superior parietal lobule concerned with multiple joint position sense, touch, and proprioceptive impulses projects throughout central and lateral regions of the rostrocaudal pons. The caudal inferior parietal lobule implicated in the neglect syndrome favors the rostral half of the pons in the lateral and dorsolateral regions [10].

Auditory association areas in the superior temporal gyrus and supratemporal plane are connected with the lateral and dorsolateral pontine nuclei. Cortices in the upper bank of the superior temporal sulcus activated during face recognition tasks project to the lateral, dorsolateral, and extreme dorsolateral pontine nuclei [14]. Motion-sensitive temporal lobe areas MT (middle temporal), FST (fundus of the superior temporal sulcus), and MST (medial superior temporal) also have pontine connections [15], but inferotemporal cortex including the rostral lower bank of the superior temporal sulcus, which is relevant for feature discrimination, has no pontine efferents. Thus, the dorsal visual (where) stream concerned with motion analysis and visual–spatial attributes of motion participates in the cerebrocerebellar interaction, but the ventral visual (what) stream governing visual object identification does not. Parastriate projections from occipitotemporal and occipitoparietal regions also respect the dorsal–ventral dichotomy. The medial and dorsal prelunate regions project to the pons (dorsolateral, lateral, and lateral aspect of the peripeduncular nuclei most heavily), but ventral prelunate cortices and inferotemporal regions do not [16]. Projections from the temporal lobe homologue of the Wernicke language area in human, together with those from the monkey homologue of Broca’s area, are relevant in the light of cerebellar activation during functional neuroimaging studies of language [17, 18] and in disorders of language following cerebellar lesions [19, 20].

Paralimbic projections arise from posterior parahippocampal gyrus important for spatial attributes of memory, directed to lateral, dorsolateral, and lateral peripeduncular nuclei. Cingulate cortex projections arise from motor areas in the depth of the cingulate sulcus [21] and from areas concerned with motivation and drive in rostral and caudal cingulate areas [22]. The anterior insular cortex, important for autonomic systems and pain modulation also has pontine connections [9]. Projections arise also from multimodal deep layers of the superior colliculus and medial mammillary bodies involved in memory and emotion [23]. The hypothalamus, critical for autonomic control and limbic behaviors, has direct reciprocal connections with the cerebellum [24].

Corticopontine projections are arranged with topographic specificity. Sensorimotor terminations are more caudally situated; association areas project more rostrally. Terminations occur in multiple patches forming interdigitating mosaics. The significance of associative corticopontine inputs in human compared with monkey is underscored by enlargement in human of the medial part of the cerebral peduncle conveying prefontopontine fibers [25], reflecting evolutionary pressure in which interconnected systems evolve in concert with each other.

Pontocerebellar Projections

The caudal pons sends sensorimotor-related information to the cerebellar anterior lobe. Rostral pontine nuclei convey cognitively relevant information to the posterior cerebellum: medial pontine projections from prefrontal cortices to crus I and to crus II, and medial, ventral, and lateral pons conveying information from parietal association cortices to crus I, crus II, and lobule VIIB. These anatomical studies extend earlier physiological conclusions that parietal and prefrontal cortices are functionally related mainly to crus I, crus II, and the paramedian lobule of the cerebellum [26]. In the pontocerebellar projection, each cerebellar folium receives input from a unique complement of pontine cell groups, some of which are widely separated [1, 27]. The pattern of diverging corticopontine projections and converging pontocerebellar projections led to the suggestion that information from one cerebral cortical area is distributed to numerous sites in the cerebellar cortex [27], although trans-synaptic viral tract tracing studies reveal that anterograde projections through the medial pons are directed to focal areas in crus I and crus II [28].

Cerebellar Feedback

Purkinje cells convey the output of the cerebellar cortex to the deep cerebellar nuclei (DCN), which send projections back to the brainstem, or to the cerebral cortex via the thalamus. The cerebellar cortex–DCN–thalamus–cerebral cortex feedback loop is arranged so that motor related interpositus nuclei (globose and emboliform in human) send efferents from cerebellar anterior lobe motor areas to the cerebral sensorimotor regions, whereas the ventral dentate sends information from the cerebellar posterior lobe to cerebral association areas—prefrontal, posterior parietal, and others [28, 29] (see Fig. 2). The cerebellar vermis and fastigial nucleus are linked with brainstem and thalamic structures concerned not only with vestibular and oculomotor control, posture, and equilibrium, but also with autonomic and paralimbic cerebral areas, consistent with the notion of the vermis and fastigial nucleus as the limbic cerebellum [3].

Fig. 2 a Diagram of the lateral view of a cebus monkey brain (top) to show the location of injections of McIntyre-B strain of herpes simplex virus I in the primary motor cortex arm representation (M1arm), ventral premotor cortex arm representation (PMVarm), and in the prefrontal cortex in areas 9 and 46. The resulting retrogradely labeled neurons (below) in the cerebellar interpositus nucleus (IP) and dentate nucleus (DN) are indicated by solid dots and show the dorsal–ventral dichotomy in dentate projections to motor versus prefrontal cortices. Adapted from [29]. b Representation on flattened views of the cerebellum of the input–output organization of cerebellar loops with motor cortex M1 (left) and area 46 (right) revealed using anterograde and retrograde strains of rabies virus as tract tracer. M1 is interconnected with lobules IV to VI; prefrontal cortical area 46 is linked predominantly with crus II. Adapted from [28] Full size image

Synthesis

Against the backdrop of the heterogenous and topographically arranged connections of the cerebellum with the rest of the neuraxis stands the essentially constant architecture of the cerebellar cortex. This dichotomy is the basis of the dysmetria of thought theory, which poses that a constant computation—the universal cerebellar transform—is applied to multiple domains of neurological function subserved by the distributed neural circuits of which cerebellum is an integral node [3]. The anatomical connections that link the cerebellum with both the external and the internal worlds thus provide the critical neural substrates of the putative cerebellar role in perception. These conclusions from tract tracing studies in the monkey are supported by resting state functional connectivity magnetic resonance imaging (MRI; [30]) and task-based functional MRI studies in humans [18], as well as by clinical investigations in patients with cerebellar damage [19].