Relationship of complex spike synchrony bands and climbing fiber projection determined by reference to aldolase C compartments in crus IIa of the rat cerebellar cortex

Abstract

Synchronous complex spike (CS) activity occurs most often among cerebellar Purkinje cells located in a narrow longitudinal (parasagittal) strip of cortex (synchrony band). The relationship of the anatomical organization of the olivocerebellar projection to these synchrony bands has not been investigated in detail. Thus, we studied this relationship by using the aldolase C (zebrin II) expression pattern, another landmark for the cerebellar longitudinal organization, as a reference frame in rat crus IIa. Crus IIa consists of 10 aldolase C-positive and -negative longitudinal compartments. Aldolase C labeling after multiple-electrode recording of CSs indicated that in lateral crus IIa (compartments 5+ to 7+) synchrony bands were generally constrained to single compartments. In contrast, in medial crus IIa (compartments 4a- to 5a-) the synchrony within and across the compartments was much higher than in lateral crus IIa, resulting in wide synchrony bands covering multiple compartments. Retrograde labeling of olivary neurons by injections of biotinylated dextran amine into aldolase C compartments in crus IIa showed that compartments in medial crus IIa were all innervated by the caudal part of the medial accessory olive. On the other hand, each aldolase C compartment in the lateral crus IIa was innervated by a region in a different subnucleus in the rostral inferior olive. These regions in different subnuclei were located close to each other. These results suggest that CS synchrony bands reflect the olivocerebellar compartmental projection pattern and neuronal coupling within a particular olivary subnucleus, and that medial and lateral crus IIa may be functionally distinct.

Spatial Pattern Coding of Sensory Information by Climbing Fiber-Evoked Calcium Signals in Networks of Neighboring Cerebellar Purkinje Cells

“…This spontaneous CS synchrony falls off over ϳ200 m mediolaterally in cerebellar cortex and is increased by sensory stimulation and harmaline administration. Because harmaline acts to enhance subthreshold oscillations in the inferior olive neurons, which give rise to the climbing fibers (de Montigny and Lamarre, 1973;Llinás et al, 1974), this suggests that local CS synchrony originates in the inferior olive, consistent with studies of climbing fiber connectivity (Sugihara et al, 2001(Sugihara et al, , 2007. Our results, obtained using a technique affording much higher spatial resolution than previously available, are in close agreement with and extend previous studies using multielectrode arrays (Yamamoto et al, 2001;Blenkinsop and Lang, 2006).…”

“…Multiple-electrode arrays typically have an intersite spacing of several hundred micrometers, and, thus, whereas CS correlation and its relationship to the anatomical zonal structure of the cerebellum is understood on a broad spatial scale (Sugihara et al, 2007), the fine-scale spatial correlation structure on the level of neighboring neurons is unknown. To examine our first question, we thus ask how synchrony falls off with mediolateral distance between cells.…”

Systematic Regional Variations in Purkinje Cell Spiking Patterns

“…Furthermore, later we present anatomical and statistically analyses in support of the validity of using the A2 and C1 zones as surrogates for Z+ and Z− bands (see later Results subsection ‘ Degree of overlap of physiologically-defined zones with zebrin bands’ ). The third dataset consists of multielectrode recordings from a prior study [36], which, because of electrode placement in the mid to upper molecular layer (see Methods), consists only of CS activity. In this dataset PC locations with respect to the zebrin bands were verified histologically as described in the Methods.…”

“…Recordings of dendritic CSs from a dataset that was used for other purposes in a previous study were also analyzed [36]. In these experiments a multielectrode recording approach was used in which CS activity was obtained from arrays of crus 2a PCs simultaneously.…”

Inferior Olive: All Ins and Outs

“…500 mm wide) that are defined by the pattern of climbing fiber innervation (Fig. 43.7) Sugihara et al 1993;Wylie et al 1995;Lang et al 1999;Sugihara et al 2007;Mukamel et al 2009;Ozden et al 2009;Schultz et al 2009;Bosman et al 2010). Two-photon Ca 2+ imaging of Purkinje cell dendrites showed that the highest degree of complex spike synchrony is found in parasagittal "microzones," which are 3-19 Purkinje cells wide (Mukamel et al 2009;Ozden et al 2009;Schultz et al 2009).…”