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Processing of visual signals related to self-motion in the cerebellum of pigeons.

Wylie DR - Front Behav Neurosci (2013)

Bottom Line: Optic flow is the visual motion that occurs across the entire retina as a result of self-motion and is processed by subcortical visual pathways that project to the cerebellum.As the tectofugal system is involved in the analysis of local motion, there is integration of optic flow and local motion information in VI-VIII.This part of the cerebellum may be important for moving through a cluttered environment.

View Article: PubMed Central - PubMed

Affiliation: Centre for Neuroscience and Department of Psychology, University of Alberta Edmonton, AB, Canada.

ABSTRACT
In this paper I describe the key features of optic flow processing in pigeons. Optic flow is the visual motion that occurs across the entire retina as a result of self-motion and is processed by subcortical visual pathways that project to the cerebellum. These pathways originate in two retinal-recipient nuclei, the nucleus of the basal optic root (nBOR) and the nucleus lentiformis mesencephali, which project to the vestibulocerebellum (VbC) (folia IXcd and X), directly as mossy fibers, and indirectly as climbing fibers from the inferior olive. Optic flow information is integrated with vestibular input in the VbC. There is a clear separation of function in the VbC: Purkinje cells in the flocculus process optic flow resulting from self-rotation, whereas Purkinje cells in the uvula/nodulus process optic flow resulting from self-translation. Furthermore, Purkinje cells with particular optic flow preferences are organized topographically into parasagittal "zones." These zones are correlated with expression of the isoenzyme aldolase C, also known as zebrin II (ZII). ZII expression is heterogeneous such that there are parasagittal stripes of Purkinje cells that have high expression (ZII+) alternating with stripes of Purkinje cells with low expression (ZII-). A functional zone spans a ZII± stripe pair. That is, each zone that contains Purkinje cells responsive to a particular pattern of optic flow is subdivided into a strip containing ZII+ Purkinje cells and a strip containing ZII- Purkinje cells. Additionally, there is optic flow input to folia VI-VIII of the cerebellum from lentiformis mesencephali. These folia also receive visual input from the tectofugal system via pontine nuclei. As the tectofugal system is involved in the analysis of local motion, there is integration of optic flow and local motion information in VI-VIII. This part of the cerebellum may be important for moving through a cluttered environment.

No MeSH data available.


Related in: MedlinePlus

(A) Shows the pattern of optic flow resulting from forward translation along the z-axis, as projected onto a sphere surrounding the bird. The arrows represent local image motion in the flowfield. (B) Shows the optic flow resulting from rotation about the z-axis (roll). (C) and (D) Show the directional tuning curves in response to large-field stimulation of the ipsi- and contralateral eyes for Purkinje cells in the vestibulocerebellum. The arrows represent the peak best fit sine wave to the tuning curve, and serves as a proxy for the preferred direction. The cell in (C) preferred backward (b) [i.e., nasal-to-temporal (n-t)] motion in both eyes, which would result from forward self-translation (adapted from Graham and Wylie, 2012). The cell in (D) preferred upward (u) motion in the ipsilateral eye, and downward motion in the contralateral eye, which results from rotation of the head about the z-axis (roll) (adapted from Wylie and Frost, 1991). The gray circles represent the spontaneous firing rates of these neurons, which is typically about 1 spikes/s. d: downward motion; f: forward motion [i.e., temporal-to-nasal (t-n)].
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Figure 3: (A) Shows the pattern of optic flow resulting from forward translation along the z-axis, as projected onto a sphere surrounding the bird. The arrows represent local image motion in the flowfield. (B) Shows the optic flow resulting from rotation about the z-axis (roll). (C) and (D) Show the directional tuning curves in response to large-field stimulation of the ipsi- and contralateral eyes for Purkinje cells in the vestibulocerebellum. The arrows represent the peak best fit sine wave to the tuning curve, and serves as a proxy for the preferred direction. The cell in (C) preferred backward (b) [i.e., nasal-to-temporal (n-t)] motion in both eyes, which would result from forward self-translation (adapted from Graham and Wylie, 2012). The cell in (D) preferred upward (u) motion in the ipsilateral eye, and downward motion in the contralateral eye, which results from rotation of the head about the z-axis (roll) (adapted from Wylie and Frost, 1991). The gray circles represent the spontaneous firing rates of these neurons, which is typically about 1 spikes/s. d: downward motion; f: forward motion [i.e., temporal-to-nasal (t-n)].

Mentions: The motion of any object through 3-dimensional space can be described with reference to its translation between two points, and its rotation about an intrinsic axis. This can also be applied to self-motion of an organism, and vertebrates do have mechanisms to detect both self-translation and self-rotation. The vestibular system consists of the semicircular canals, which detect head rotation, and the otolith organs, which detect head acceleration resulting from gravity and self-translation (Wilson and Melvill Jones, 1979). A neural system involved in analyzing optic flow can also encode self-translation and self-rotation. The patterns of optic flow resulting from self-translation and self-rotation are quite different. Figures 3A and B show, respectively, the patterns of optic flow resulting from translation along, and rotation about, the z-axis. These are shown as projected onto imaginary spheres surrounding the animal, where the arrows indicate local motion within the flowfield (Gibson, 1954). Assuming no eye movements, during self-translation there is a focus of expansion in the direction of self-motion, and backward motion along the equator of this sphere in both visual fields (Figure 3A). Not visible in the figure, there would also be a focus of contraction behind the animal's head. For self-rotation about the z-axis, there is circular motion about the axis of rotation, but along the equator of this sphere there is upward and downward motion in the right and left visual fields respectively. Although the neurons in LM and nBOR have large receptive fields for analyzing optic flow, they cannot distinguish optic flow patterns resulting from self-rotation and self-translation. For example, a neuron preferring upward motion, such as that depicted in Figures 2C–E, would respond equally well to downward-translation and a rightward roll of the head. For a predominantly lateral-eyed animal such as a pigeon, a simple solution is to integrate information from the ipsi- and contralateral visual fields. This is what occurs in the olivo-vestibulocerebellar pathway shown in blue in Figure 1. In Figures 3C and D, examples are shown from the VbC on the left side of the brain, where directional tuning to largefield moving stimuli was measured for both the ipsilateral and contralateral eyes. The neuron in Figure 3C responded best to backward (nasal-to-temporal) motion in both eyes, which would result from forward self-translation. The neuron in Figure 3D responded best to upward motion in the ipsilateral eye, and downward motion in the contralateral eye, which would result from a rightward rotation about the z-axis (roll). Although there are a few neurons in nBOR, LM, and the ventral tegmental area (VTA) that have such binocular receptive fields that respond to particular patterns of optic flow resulting from self-translation and self-rotation (Wylie and Frost, 1990b, 1999b; Wylie, 2000), almost all neurons in mcIO and the VbC have panoramic receptive fields (Wylie and Frost, 1991, 1993, 1999a; Wylie et al., 1993; Winship and Wylie, 2001). Moreover there is a clear topographic organization of neurons responsive to translational and rotational optic flow (Winship and Wylie, 2001; Pakan et al., 2005; Graham and Wylie, 2012).


Processing of visual signals related to self-motion in the cerebellum of pigeons.

Wylie DR - Front Behav Neurosci (2013)

(A) Shows the pattern of optic flow resulting from forward translation along the z-axis, as projected onto a sphere surrounding the bird. The arrows represent local image motion in the flowfield. (B) Shows the optic flow resulting from rotation about the z-axis (roll). (C) and (D) Show the directional tuning curves in response to large-field stimulation of the ipsi- and contralateral eyes for Purkinje cells in the vestibulocerebellum. The arrows represent the peak best fit sine wave to the tuning curve, and serves as a proxy for the preferred direction. The cell in (C) preferred backward (b) [i.e., nasal-to-temporal (n-t)] motion in both eyes, which would result from forward self-translation (adapted from Graham and Wylie, 2012). The cell in (D) preferred upward (u) motion in the ipsilateral eye, and downward motion in the contralateral eye, which results from rotation of the head about the z-axis (roll) (adapted from Wylie and Frost, 1991). The gray circles represent the spontaneous firing rates of these neurons, which is typically about 1 spikes/s. d: downward motion; f: forward motion [i.e., temporal-to-nasal (t-n)].
© Copyright Policy - open-access
Related In: Results  -  Collection

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Figure 3: (A) Shows the pattern of optic flow resulting from forward translation along the z-axis, as projected onto a sphere surrounding the bird. The arrows represent local image motion in the flowfield. (B) Shows the optic flow resulting from rotation about the z-axis (roll). (C) and (D) Show the directional tuning curves in response to large-field stimulation of the ipsi- and contralateral eyes for Purkinje cells in the vestibulocerebellum. The arrows represent the peak best fit sine wave to the tuning curve, and serves as a proxy for the preferred direction. The cell in (C) preferred backward (b) [i.e., nasal-to-temporal (n-t)] motion in both eyes, which would result from forward self-translation (adapted from Graham and Wylie, 2012). The cell in (D) preferred upward (u) motion in the ipsilateral eye, and downward motion in the contralateral eye, which results from rotation of the head about the z-axis (roll) (adapted from Wylie and Frost, 1991). The gray circles represent the spontaneous firing rates of these neurons, which is typically about 1 spikes/s. d: downward motion; f: forward motion [i.e., temporal-to-nasal (t-n)].
Mentions: The motion of any object through 3-dimensional space can be described with reference to its translation between two points, and its rotation about an intrinsic axis. This can also be applied to self-motion of an organism, and vertebrates do have mechanisms to detect both self-translation and self-rotation. The vestibular system consists of the semicircular canals, which detect head rotation, and the otolith organs, which detect head acceleration resulting from gravity and self-translation (Wilson and Melvill Jones, 1979). A neural system involved in analyzing optic flow can also encode self-translation and self-rotation. The patterns of optic flow resulting from self-translation and self-rotation are quite different. Figures 3A and B show, respectively, the patterns of optic flow resulting from translation along, and rotation about, the z-axis. These are shown as projected onto imaginary spheres surrounding the animal, where the arrows indicate local motion within the flowfield (Gibson, 1954). Assuming no eye movements, during self-translation there is a focus of expansion in the direction of self-motion, and backward motion along the equator of this sphere in both visual fields (Figure 3A). Not visible in the figure, there would also be a focus of contraction behind the animal's head. For self-rotation about the z-axis, there is circular motion about the axis of rotation, but along the equator of this sphere there is upward and downward motion in the right and left visual fields respectively. Although the neurons in LM and nBOR have large receptive fields for analyzing optic flow, they cannot distinguish optic flow patterns resulting from self-rotation and self-translation. For example, a neuron preferring upward motion, such as that depicted in Figures 2C–E, would respond equally well to downward-translation and a rightward roll of the head. For a predominantly lateral-eyed animal such as a pigeon, a simple solution is to integrate information from the ipsi- and contralateral visual fields. This is what occurs in the olivo-vestibulocerebellar pathway shown in blue in Figure 1. In Figures 3C and D, examples are shown from the VbC on the left side of the brain, where directional tuning to largefield moving stimuli was measured for both the ipsilateral and contralateral eyes. The neuron in Figure 3C responded best to backward (nasal-to-temporal) motion in both eyes, which would result from forward self-translation. The neuron in Figure 3D responded best to upward motion in the ipsilateral eye, and downward motion in the contralateral eye, which would result from a rightward rotation about the z-axis (roll). Although there are a few neurons in nBOR, LM, and the ventral tegmental area (VTA) that have such binocular receptive fields that respond to particular patterns of optic flow resulting from self-translation and self-rotation (Wylie and Frost, 1990b, 1999b; Wylie, 2000), almost all neurons in mcIO and the VbC have panoramic receptive fields (Wylie and Frost, 1991, 1993, 1999a; Wylie et al., 1993; Winship and Wylie, 2001). Moreover there is a clear topographic organization of neurons responsive to translational and rotational optic flow (Winship and Wylie, 2001; Pakan et al., 2005; Graham and Wylie, 2012).

Bottom Line: Optic flow is the visual motion that occurs across the entire retina as a result of self-motion and is processed by subcortical visual pathways that project to the cerebellum.As the tectofugal system is involved in the analysis of local motion, there is integration of optic flow and local motion information in VI-VIII.This part of the cerebellum may be important for moving through a cluttered environment.

View Article: PubMed Central - PubMed

Affiliation: Centre for Neuroscience and Department of Psychology, University of Alberta Edmonton, AB, Canada.

ABSTRACT
In this paper I describe the key features of optic flow processing in pigeons. Optic flow is the visual motion that occurs across the entire retina as a result of self-motion and is processed by subcortical visual pathways that project to the cerebellum. These pathways originate in two retinal-recipient nuclei, the nucleus of the basal optic root (nBOR) and the nucleus lentiformis mesencephali, which project to the vestibulocerebellum (VbC) (folia IXcd and X), directly as mossy fibers, and indirectly as climbing fibers from the inferior olive. Optic flow information is integrated with vestibular input in the VbC. There is a clear separation of function in the VbC: Purkinje cells in the flocculus process optic flow resulting from self-rotation, whereas Purkinje cells in the uvula/nodulus process optic flow resulting from self-translation. Furthermore, Purkinje cells with particular optic flow preferences are organized topographically into parasagittal "zones." These zones are correlated with expression of the isoenzyme aldolase C, also known as zebrin II (ZII). ZII expression is heterogeneous such that there are parasagittal stripes of Purkinje cells that have high expression (ZII+) alternating with stripes of Purkinje cells with low expression (ZII-). A functional zone spans a ZII± stripe pair. That is, each zone that contains Purkinje cells responsive to a particular pattern of optic flow is subdivided into a strip containing ZII+ Purkinje cells and a strip containing ZII- Purkinje cells. Additionally, there is optic flow input to folia VI-VIII of the cerebellum from lentiformis mesencephali. These folia also receive visual input from the tectofugal system via pontine nuclei. As the tectofugal system is involved in the analysis of local motion, there is integration of optic flow and local motion information in VI-VIII. This part of the cerebellum may be important for moving through a cluttered environment.

No MeSH data available.


Related in: MedlinePlus