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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

Relationship between the optic flow zones and the zebrin II (ZII) stripes in the pigeon vestibulocerebellum (VbC). (A–H) Show results from a single experiment. (A) Shows the surface of the exposed flocculus. This is the superimposition of six photos, such that the locations of six injection electrodes (C–H) filled with either red biotinylated dextran amine (BDA) (D,F,H) or green BDA (C,E,G) are shown. (B) Shows the subsequently perfused and dissected brain. Traces of the six injections can clearly be seen on the surface of IXcd. (C–H) Show coronal sections through the VbC that have been immunoreacted for ZII to illustrate the locations of all the injections in particular ZII stripes (from Pakan et al., 2011). (I) Shows our efforts to determine the locations of the translational optic flow zones relative to the ZII stripes in IXcd (Graham and Wylie, 2012). Collapsed from several recording experiments, the recording sites of Contraction (light blue), Expansion (purple), Ascent (green), and Descent (orange) cells are indicated, as well as some cells not modulated to visual stimuli (NM; yellow) and a few VA cells (dark blue). (J) Shows a summary of how the rotational and translational optic flow neurons are organized with respect to the ZII stripes. See text for additional details. ?: Small immunopositive satellite band one to two Purkinje cells wide in the middle of P1−; AC: anterior canal; m, l, r, and c: medial, lateral, rostral, and caudal. Scale bars: (A,B) = 1 mm; (C–H) = 300 μm; (J) = 500 μm.
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Figure 9: Relationship between the optic flow zones and the zebrin II (ZII) stripes in the pigeon vestibulocerebellum (VbC). (A–H) Show results from a single experiment. (A) Shows the surface of the exposed flocculus. This is the superimposition of six photos, such that the locations of six injection electrodes (C–H) filled with either red biotinylated dextran amine (BDA) (D,F,H) or green BDA (C,E,G) are shown. (B) Shows the subsequently perfused and dissected brain. Traces of the six injections can clearly be seen on the surface of IXcd. (C–H) Show coronal sections through the VbC that have been immunoreacted for ZII to illustrate the locations of all the injections in particular ZII stripes (from Pakan et al., 2011). (I) Shows our efforts to determine the locations of the translational optic flow zones relative to the ZII stripes in IXcd (Graham and Wylie, 2012). Collapsed from several recording experiments, the recording sites of Contraction (light blue), Expansion (purple), Ascent (green), and Descent (orange) cells are indicated, as well as some cells not modulated to visual stimuli (NM; yellow) and a few VA cells (dark blue). (J) Shows a summary of how the rotational and translational optic flow neurons are organized with respect to the ZII stripes. See text for additional details. ?: Small immunopositive satellite band one to two Purkinje cells wide in the middle of P1−; AC: anterior canal; m, l, r, and c: medial, lateral, rostral, and caudal. Scale bars: (A,B) = 1 mm; (C–H) = 300 μm; (J) = 500 μm.

Mentions: The ZII stripes are apparent in folium IXcd of the pigeon VbC (Pakan et al., 2007; Figures 8B–D). However, in folium X there are no ZII stripes, as all the Purkinje cells are ZII+ve (Figures 8C and D). There are seven stripe pairs in IXcd numbered, from the midline, P1± to P7±. Importantly, the P1± stripe is divided into medial and lateral halves (P1− med, P1− lat) by a thin ZII+ stripe that is only 1–3 Purkinje cells wide (see “?” in Figures 8C and D). Also, the P2+ stripe is divided into medial and lateral halves (P2+ med, P2+ lat) by a thin ZII−ve notch (see inverted triangle in Figure 8C). In a recent series of studies (Pakan and Wylie, 2008; Pakan et al., 2011; Graham and Wylie, 2012), we have attempted to determine if the ZII stripes are correlated with the optic flow zones in the VbC. We found a clear relationship: each optic flow zone spans a ZII+ve/−ve stripe pair. Data regarding the floccular zones is shown in Figures 9A–H, from our most comprehensive case (Pakan et al., 2011). The procedure was to record from identified HA and VA neurons, mark the recording sites with an injection of red or green fluorescent tracer (biotinylated dextran amine; BDA), then subsequently process the tissue for ZII to determine the location of the recordings. Figure 9A shows the view of the flocculus through the surgical microscope with six injection pipettes superimposed. Those marked C, E, and G contained green BDA, whereas the others contained red BDA. When the perfused brain was dissected, the six injections could be clearly seen under a dissecting microscope (Figure 9B). At sites C, F, and G, VA neurons were recorded, whereas HA neurons were recorded at sites D, E, and H. As shown in the corresponding panels with the ZII expression pattern visualized in coronal sections, VA injections were localized to stripes P4+ (Figure 9C), P6+ (Figure 9F), and P6− (Figure 9G), whereas HA injections were found in stripes P5+ (Figure 9D), P5− (Figure 9E), and P7− (Figure 7H). Supplemented with data from other cases, we determined that the medial and lateral VA zones spanned the P4± and P6± stripe pairs, respectively, and the medial and lateral HA zones spanned the P5± and P7± stripe pairs, respectively (see Figure 9J). A similar story emerged for the translation optic flow zones in the uvula. Figure 9I shows the locations of identified neurons superimposed on the ZII stripes in IXcd from several cases (Graham and Wylie, 2012). The Contraction cells were localized to the P1+ and P1−med stripes, and the Descent cells were localized to the P2+lat and P2− stripes. Ascent and Expansion cells were found intermingled in the P2+med and P1−lat stripes. We did localize some cells to the P3+ stripe, but these were not modulated by the optic flow stimuli. The relationship between the ZII stripes and the optic flow zones in the VbC is summarized in Figure 9J. Each ZII+ve/−ve stripe pair spans an optic flow zone. Each one of these optic flow zones contains neurons with the same optic flow preference, with the exception of the one zone that contains both Ascent and Expansion neurons. Why this zone is peculiar in this regard is unknown, as is the function of the P3± stripe pair.


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

Wylie DR - Front Behav Neurosci (2013)

Relationship between the optic flow zones and the zebrin II (ZII) stripes in the pigeon vestibulocerebellum (VbC). (A–H) Show results from a single experiment. (A) Shows the surface of the exposed flocculus. This is the superimposition of six photos, such that the locations of six injection electrodes (C–H) filled with either red biotinylated dextran amine (BDA) (D,F,H) or green BDA (C,E,G) are shown. (B) Shows the subsequently perfused and dissected brain. Traces of the six injections can clearly be seen on the surface of IXcd. (C–H) Show coronal sections through the VbC that have been immunoreacted for ZII to illustrate the locations of all the injections in particular ZII stripes (from Pakan et al., 2011). (I) Shows our efforts to determine the locations of the translational optic flow zones relative to the ZII stripes in IXcd (Graham and Wylie, 2012). Collapsed from several recording experiments, the recording sites of Contraction (light blue), Expansion (purple), Ascent (green), and Descent (orange) cells are indicated, as well as some cells not modulated to visual stimuli (NM; yellow) and a few VA cells (dark blue). (J) Shows a summary of how the rotational and translational optic flow neurons are organized with respect to the ZII stripes. See text for additional details. ?: Small immunopositive satellite band one to two Purkinje cells wide in the middle of P1−; AC: anterior canal; m, l, r, and c: medial, lateral, rostral, and caudal. Scale bars: (A,B) = 1 mm; (C–H) = 300 μm; (J) = 500 μm.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
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Figure 9: Relationship between the optic flow zones and the zebrin II (ZII) stripes in the pigeon vestibulocerebellum (VbC). (A–H) Show results from a single experiment. (A) Shows the surface of the exposed flocculus. This is the superimposition of six photos, such that the locations of six injection electrodes (C–H) filled with either red biotinylated dextran amine (BDA) (D,F,H) or green BDA (C,E,G) are shown. (B) Shows the subsequently perfused and dissected brain. Traces of the six injections can clearly be seen on the surface of IXcd. (C–H) Show coronal sections through the VbC that have been immunoreacted for ZII to illustrate the locations of all the injections in particular ZII stripes (from Pakan et al., 2011). (I) Shows our efforts to determine the locations of the translational optic flow zones relative to the ZII stripes in IXcd (Graham and Wylie, 2012). Collapsed from several recording experiments, the recording sites of Contraction (light blue), Expansion (purple), Ascent (green), and Descent (orange) cells are indicated, as well as some cells not modulated to visual stimuli (NM; yellow) and a few VA cells (dark blue). (J) Shows a summary of how the rotational and translational optic flow neurons are organized with respect to the ZII stripes. See text for additional details. ?: Small immunopositive satellite band one to two Purkinje cells wide in the middle of P1−; AC: anterior canal; m, l, r, and c: medial, lateral, rostral, and caudal. Scale bars: (A,B) = 1 mm; (C–H) = 300 μm; (J) = 500 μm.
Mentions: The ZII stripes are apparent in folium IXcd of the pigeon VbC (Pakan et al., 2007; Figures 8B–D). However, in folium X there are no ZII stripes, as all the Purkinje cells are ZII+ve (Figures 8C and D). There are seven stripe pairs in IXcd numbered, from the midline, P1± to P7±. Importantly, the P1± stripe is divided into medial and lateral halves (P1− med, P1− lat) by a thin ZII+ stripe that is only 1–3 Purkinje cells wide (see “?” in Figures 8C and D). Also, the P2+ stripe is divided into medial and lateral halves (P2+ med, P2+ lat) by a thin ZII−ve notch (see inverted triangle in Figure 8C). In a recent series of studies (Pakan and Wylie, 2008; Pakan et al., 2011; Graham and Wylie, 2012), we have attempted to determine if the ZII stripes are correlated with the optic flow zones in the VbC. We found a clear relationship: each optic flow zone spans a ZII+ve/−ve stripe pair. Data regarding the floccular zones is shown in Figures 9A–H, from our most comprehensive case (Pakan et al., 2011). The procedure was to record from identified HA and VA neurons, mark the recording sites with an injection of red or green fluorescent tracer (biotinylated dextran amine; BDA), then subsequently process the tissue for ZII to determine the location of the recordings. Figure 9A shows the view of the flocculus through the surgical microscope with six injection pipettes superimposed. Those marked C, E, and G contained green BDA, whereas the others contained red BDA. When the perfused brain was dissected, the six injections could be clearly seen under a dissecting microscope (Figure 9B). At sites C, F, and G, VA neurons were recorded, whereas HA neurons were recorded at sites D, E, and H. As shown in the corresponding panels with the ZII expression pattern visualized in coronal sections, VA injections were localized to stripes P4+ (Figure 9C), P6+ (Figure 9F), and P6− (Figure 9G), whereas HA injections were found in stripes P5+ (Figure 9D), P5− (Figure 9E), and P7− (Figure 7H). Supplemented with data from other cases, we determined that the medial and lateral VA zones spanned the P4± and P6± stripe pairs, respectively, and the medial and lateral HA zones spanned the P5± and P7± stripe pairs, respectively (see Figure 9J). A similar story emerged for the translation optic flow zones in the uvula. Figure 9I shows the locations of identified neurons superimposed on the ZII stripes in IXcd from several cases (Graham and Wylie, 2012). The Contraction cells were localized to the P1+ and P1−med stripes, and the Descent cells were localized to the P2+lat and P2− stripes. Ascent and Expansion cells were found intermingled in the P2+med and P1−lat stripes. We did localize some cells to the P3+ stripe, but these were not modulated by the optic flow stimuli. The relationship between the ZII stripes and the optic flow zones in the VbC is summarized in Figure 9J. Each ZII+ve/−ve stripe pair spans an optic flow zone. Each one of these optic flow zones contains neurons with the same optic flow preference, with the exception of the one zone that contains both Ascent and Expansion neurons. Why this zone is peculiar in this regard is unknown, as is the function of the P3± stripe pair.

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