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Features of the retinotopic representation in the visual wulst of a laterally eyed bird, the zebra finch (Taeniopygia guttata).

Michael N, Löwel S, Bischof HJ - PLoS ONE (2015)

Bottom Line: We found that the visual wulst can be activated by visual stimuli from a large part of the visual field of the contralateral eye.This confirms earlier electrophysiological studies indicating an inhibitory influence of the activation of the ipsilateral eye on wulst activity elicited by stimulating the contralateral eye.Instead, this brain area may be involved in the processing of visual information necessary for spatial orientation.

View Article: PubMed Central - PubMed

Affiliation: Department of Systems Neuroscience, Johann-Friedrich-Blumenbach Institut für Zoologie und Anthropologie, Universität Göttingen, Göttingen, Germany; Göttingen Graduate School for Neurosciences, Biophysics, and Molecular Biosciences (GGNB), Göttingen, Germany.

ABSTRACT
The visual wulst of the zebra finch comprises at least two retinotopic maps of the contralateral eye. As yet, it is not known how much of the visual field is represented in the wulst neuronal maps, how the organization of the maps is related to the retinal architecture, and how information from the ipsilateral eye is involved in the activation of the wulst. Here, we have used autofluorescent flavoprotein imaging and classical anatomical methods to investigate such characteristics of the most posterior map of the multiple retinotopic representations. We found that the visual wulst can be activated by visual stimuli from a large part of the visual field of the contralateral eye. Horizontally, the visual field representation extended from -5° beyond the beak tip up to +125° laterally. Vertically, a small strip from -10° below to about +25° above the horizon activated the visual wulst. Although retinal ganglion cells had a much higher density around the fovea and along a strip extending from the fovea towards the beak tip, these areas were not overrepresented in the wulst map. The wulst area activated from the foveal region of the ipsilateral eye, overlapped substantially with the middle of the three contralaterally activated regions in the visual wulst, and partially with the other two. Visual wulst activity evoked by stimulation of the frontal visual field was stronger with contralateral than with binocular stimulation. This confirms earlier electrophysiological studies indicating an inhibitory influence of the activation of the ipsilateral eye on wulst activity elicited by stimulating the contralateral eye. The lack of a foveal overrepresentation suggests that identification of objects may not be the primary task of the zebra finch visual wulst. Instead, this brain area may be involved in the processing of visual information necessary for spatial orientation.

No MeSH data available.


Related in: MedlinePlus

Simultaneous input from both eyes reduces the contralateral eye evoked activity in the visual wulst.Examples from two birds for the azimuth and elevation maps obtained by visually stimulating contralateral and the ipsilateral eye, when stimulated from an angle of 0° (frontal direction) and also the maps obtained when both eyes were open are shown. The magnitude of activity is represented as a number in the upper right corner of the grey scale activity map. The schematic representation of the stimulus used is shown on the left side of the corresponding maps and the distance of the middle of the monitor was always maintained as 30 cm. A-C and D-F—The azimuth activity map obtained respectively when the contralateral, ipsilateral and both eyes simultaneously, were stimulated with an azimuth stimulus at 0° with respect to the beak, from two birds. Ipsilaterally evoked activity was always lower when compared to that of the contralateral eye (compare A and B and D and E). Simultaneous input from both eyes reduces the contralaterally evoked activity in the visual wulst (compare A and C and D and F). G-I and J-L—The elevation activity map obtained respectively when the contralateral, ipsilateral and both eyes simultaneously, were stimulated with an elevation stimulus at 0° with respect to the beak. Similar to the azimuth result, ipsilateral eye showed very feebly evoked activity in the visual wulst when compared to the contralateral eye (compare G and H, J and K). Simultaneous input from both eyes reduces the contralaterally evoked activity in the visual wulst (compare G and I, J and L). M—Difference in the magnitude of wulst activation when the contralateral eye was stimulated alone and both ipsilateral and contralateral eyes were simultaneously stimulated with an azimuth stimulus. N—Difference in the magnitude of wulst activation when the contralateral eye was stimulated alone and both ipsilateral and contralateral eyes were simultaneously stimulated with an elevation stimulus. In both azimuth and elevation stimulation, there was a significant difference in the activity evoked by contralateral eye stimulation and simultaneous stimulation of both eyes. O—Difference in the average wulst activation, when the contralateral eye was stimulated alone and both ipsilateral and contralateral eyes were simultaneously stimulated with an azimuth stimulus. P—Difference in the average wulst activation, when the contralateral eye was stimulated alone and both ipsilateral and contralateral eyes were simultaneously stimulated with an elevation stimulus. The blue and green rectangular boxes around the maps indicate the examples chosen from the graphs shown below. Scale bar = 500 μm.
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pone.0124917.g010: Simultaneous input from both eyes reduces the contralateral eye evoked activity in the visual wulst.Examples from two birds for the azimuth and elevation maps obtained by visually stimulating contralateral and the ipsilateral eye, when stimulated from an angle of 0° (frontal direction) and also the maps obtained when both eyes were open are shown. The magnitude of activity is represented as a number in the upper right corner of the grey scale activity map. The schematic representation of the stimulus used is shown on the left side of the corresponding maps and the distance of the middle of the monitor was always maintained as 30 cm. A-C and D-F—The azimuth activity map obtained respectively when the contralateral, ipsilateral and both eyes simultaneously, were stimulated with an azimuth stimulus at 0° with respect to the beak, from two birds. Ipsilaterally evoked activity was always lower when compared to that of the contralateral eye (compare A and B and D and E). Simultaneous input from both eyes reduces the contralaterally evoked activity in the visual wulst (compare A and C and D and F). G-I and J-L—The elevation activity map obtained respectively when the contralateral, ipsilateral and both eyes simultaneously, were stimulated with an elevation stimulus at 0° with respect to the beak. Similar to the azimuth result, ipsilateral eye showed very feebly evoked activity in the visual wulst when compared to the contralateral eye (compare G and H, J and K). Simultaneous input from both eyes reduces the contralaterally evoked activity in the visual wulst (compare G and I, J and L). M—Difference in the magnitude of wulst activation when the contralateral eye was stimulated alone and both ipsilateral and contralateral eyes were simultaneously stimulated with an azimuth stimulus. N—Difference in the magnitude of wulst activation when the contralateral eye was stimulated alone and both ipsilateral and contralateral eyes were simultaneously stimulated with an elevation stimulus. In both azimuth and elevation stimulation, there was a significant difference in the activity evoked by contralateral eye stimulation and simultaneous stimulation of both eyes. O—Difference in the average wulst activation, when the contralateral eye was stimulated alone and both ipsilateral and contralateral eyes were simultaneously stimulated with an azimuth stimulus. P—Difference in the average wulst activation, when the contralateral eye was stimulated alone and both ipsilateral and contralateral eyes were simultaneously stimulated with an elevation stimulus. The blue and green rectangular boxes around the maps indicate the examples chosen from the graphs shown below. Scale bar = 500 μm.

Mentions: After having shown that visual stimuli positioned about 40 to50° laterally and -5-+25° vertically to the ipsilateral eye can activate the visual wulst, we next tested whether there is also a binocular wulst region activated from the frontal visual field, as present in mammals, and what effect binocular visual stimulation had on wulst activity. Six zebra finches were used for this experiment. The stimulus monitor was centered at 0°, in front of the beak. Both horizontal and vertical moving bars induced activity in approximately the same wulst location of the posterior map (compare Fig 10A with 10G, and 10D with 10J). Ipsilateral eye stimulation elicited only weak wulst activation in bird 5 (Fig 8B and 8H) and no discernable activation in bird 6 (Fig 10E and 10K). Interestingly, however, in both birds, binocular visual stimulation induced a wulst activation that was reduced compared to stimulation with the contralateral eye only (compare Fig 10A/10G with 10C/10I, and 10D/10J with 10F/10L). The average wulst activation after contralateral stimulation with an azimuth stimulus decreased from 1.98±0.27 (contra only) to 1.73±0.23 (contra+ipsi) (p<0.05, t-test, n = 6, Fig 10M) with binocular stimulation, and from 2.54±0.35 (contra only) to 2.24±0.39 (contra+ipsi) (p<0.05, t-test, n = 6, Fig 10N) for elevation. Thus, the ipsilateral eye exerted a measurable inhibitory influence on wulst activity when both eyes were stimulated together in the frontal visual field. As proposed for the whole wulst area based on previous electrophysiological results [34], contralaterally evoked activity was thus reduced if there was an additional input from the ipsilateral eye. As an additional parameter to test the relation between the contralaterally evoked activity and activity evoked by simultaneous stimulation of both eyes, we calculated the average wulst activity in a region including the activity patches evoked by both azimuth and elevation stimuli using the ImageJ software (see materials and methods). Similar to the activity measurements described above, there was a significant difference between the two conditions (azimuth: contralateral: 73±8.4, contra+ipsi: 59.1±7.1, p<0.05, t-test, n = 6, Fig 10O; elevation: contralateral: 95.4±11.9, contra+ipsi: 78.4±12.9; p<0.01, t-test, n = 6, Fig 10P).


Features of the retinotopic representation in the visual wulst of a laterally eyed bird, the zebra finch (Taeniopygia guttata).

Michael N, Löwel S, Bischof HJ - PLoS ONE (2015)

Simultaneous input from both eyes reduces the contralateral eye evoked activity in the visual wulst.Examples from two birds for the azimuth and elevation maps obtained by visually stimulating contralateral and the ipsilateral eye, when stimulated from an angle of 0° (frontal direction) and also the maps obtained when both eyes were open are shown. The magnitude of activity is represented as a number in the upper right corner of the grey scale activity map. The schematic representation of the stimulus used is shown on the left side of the corresponding maps and the distance of the middle of the monitor was always maintained as 30 cm. A-C and D-F—The azimuth activity map obtained respectively when the contralateral, ipsilateral and both eyes simultaneously, were stimulated with an azimuth stimulus at 0° with respect to the beak, from two birds. Ipsilaterally evoked activity was always lower when compared to that of the contralateral eye (compare A and B and D and E). Simultaneous input from both eyes reduces the contralaterally evoked activity in the visual wulst (compare A and C and D and F). G-I and J-L—The elevation activity map obtained respectively when the contralateral, ipsilateral and both eyes simultaneously, were stimulated with an elevation stimulus at 0° with respect to the beak. Similar to the azimuth result, ipsilateral eye showed very feebly evoked activity in the visual wulst when compared to the contralateral eye (compare G and H, J and K). Simultaneous input from both eyes reduces the contralaterally evoked activity in the visual wulst (compare G and I, J and L). M—Difference in the magnitude of wulst activation when the contralateral eye was stimulated alone and both ipsilateral and contralateral eyes were simultaneously stimulated with an azimuth stimulus. N—Difference in the magnitude of wulst activation when the contralateral eye was stimulated alone and both ipsilateral and contralateral eyes were simultaneously stimulated with an elevation stimulus. In both azimuth and elevation stimulation, there was a significant difference in the activity evoked by contralateral eye stimulation and simultaneous stimulation of both eyes. O—Difference in the average wulst activation, when the contralateral eye was stimulated alone and both ipsilateral and contralateral eyes were simultaneously stimulated with an azimuth stimulus. P—Difference in the average wulst activation, when the contralateral eye was stimulated alone and both ipsilateral and contralateral eyes were simultaneously stimulated with an elevation stimulus. The blue and green rectangular boxes around the maps indicate the examples chosen from the graphs shown below. Scale bar = 500 μm.
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Related In: Results  -  Collection

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Show All Figures
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pone.0124917.g010: Simultaneous input from both eyes reduces the contralateral eye evoked activity in the visual wulst.Examples from two birds for the azimuth and elevation maps obtained by visually stimulating contralateral and the ipsilateral eye, when stimulated from an angle of 0° (frontal direction) and also the maps obtained when both eyes were open are shown. The magnitude of activity is represented as a number in the upper right corner of the grey scale activity map. The schematic representation of the stimulus used is shown on the left side of the corresponding maps and the distance of the middle of the monitor was always maintained as 30 cm. A-C and D-F—The azimuth activity map obtained respectively when the contralateral, ipsilateral and both eyes simultaneously, were stimulated with an azimuth stimulus at 0° with respect to the beak, from two birds. Ipsilaterally evoked activity was always lower when compared to that of the contralateral eye (compare A and B and D and E). Simultaneous input from both eyes reduces the contralaterally evoked activity in the visual wulst (compare A and C and D and F). G-I and J-L—The elevation activity map obtained respectively when the contralateral, ipsilateral and both eyes simultaneously, were stimulated with an elevation stimulus at 0° with respect to the beak. Similar to the azimuth result, ipsilateral eye showed very feebly evoked activity in the visual wulst when compared to the contralateral eye (compare G and H, J and K). Simultaneous input from both eyes reduces the contralaterally evoked activity in the visual wulst (compare G and I, J and L). M—Difference in the magnitude of wulst activation when the contralateral eye was stimulated alone and both ipsilateral and contralateral eyes were simultaneously stimulated with an azimuth stimulus. N—Difference in the magnitude of wulst activation when the contralateral eye was stimulated alone and both ipsilateral and contralateral eyes were simultaneously stimulated with an elevation stimulus. In both azimuth and elevation stimulation, there was a significant difference in the activity evoked by contralateral eye stimulation and simultaneous stimulation of both eyes. O—Difference in the average wulst activation, when the contralateral eye was stimulated alone and both ipsilateral and contralateral eyes were simultaneously stimulated with an azimuth stimulus. P—Difference in the average wulst activation, when the contralateral eye was stimulated alone and both ipsilateral and contralateral eyes were simultaneously stimulated with an elevation stimulus. The blue and green rectangular boxes around the maps indicate the examples chosen from the graphs shown below. Scale bar = 500 μm.
Mentions: After having shown that visual stimuli positioned about 40 to50° laterally and -5-+25° vertically to the ipsilateral eye can activate the visual wulst, we next tested whether there is also a binocular wulst region activated from the frontal visual field, as present in mammals, and what effect binocular visual stimulation had on wulst activity. Six zebra finches were used for this experiment. The stimulus monitor was centered at 0°, in front of the beak. Both horizontal and vertical moving bars induced activity in approximately the same wulst location of the posterior map (compare Fig 10A with 10G, and 10D with 10J). Ipsilateral eye stimulation elicited only weak wulst activation in bird 5 (Fig 8B and 8H) and no discernable activation in bird 6 (Fig 10E and 10K). Interestingly, however, in both birds, binocular visual stimulation induced a wulst activation that was reduced compared to stimulation with the contralateral eye only (compare Fig 10A/10G with 10C/10I, and 10D/10J with 10F/10L). The average wulst activation after contralateral stimulation with an azimuth stimulus decreased from 1.98±0.27 (contra only) to 1.73±0.23 (contra+ipsi) (p<0.05, t-test, n = 6, Fig 10M) with binocular stimulation, and from 2.54±0.35 (contra only) to 2.24±0.39 (contra+ipsi) (p<0.05, t-test, n = 6, Fig 10N) for elevation. Thus, the ipsilateral eye exerted a measurable inhibitory influence on wulst activity when both eyes were stimulated together in the frontal visual field. As proposed for the whole wulst area based on previous electrophysiological results [34], contralaterally evoked activity was thus reduced if there was an additional input from the ipsilateral eye. As an additional parameter to test the relation between the contralaterally evoked activity and activity evoked by simultaneous stimulation of both eyes, we calculated the average wulst activity in a region including the activity patches evoked by both azimuth and elevation stimuli using the ImageJ software (see materials and methods). Similar to the activity measurements described above, there was a significant difference between the two conditions (azimuth: contralateral: 73±8.4, contra+ipsi: 59.1±7.1, p<0.05, t-test, n = 6, Fig 10O; elevation: contralateral: 95.4±11.9, contra+ipsi: 78.4±12.9; p<0.01, t-test, n = 6, Fig 10P).

Bottom Line: We found that the visual wulst can be activated by visual stimuli from a large part of the visual field of the contralateral eye.This confirms earlier electrophysiological studies indicating an inhibitory influence of the activation of the ipsilateral eye on wulst activity elicited by stimulating the contralateral eye.Instead, this brain area may be involved in the processing of visual information necessary for spatial orientation.

View Article: PubMed Central - PubMed

Affiliation: Department of Systems Neuroscience, Johann-Friedrich-Blumenbach Institut für Zoologie und Anthropologie, Universität Göttingen, Göttingen, Germany; Göttingen Graduate School for Neurosciences, Biophysics, and Molecular Biosciences (GGNB), Göttingen, Germany.

ABSTRACT
The visual wulst of the zebra finch comprises at least two retinotopic maps of the contralateral eye. As yet, it is not known how much of the visual field is represented in the wulst neuronal maps, how the organization of the maps is related to the retinal architecture, and how information from the ipsilateral eye is involved in the activation of the wulst. Here, we have used autofluorescent flavoprotein imaging and classical anatomical methods to investigate such characteristics of the most posterior map of the multiple retinotopic representations. We found that the visual wulst can be activated by visual stimuli from a large part of the visual field of the contralateral eye. Horizontally, the visual field representation extended from -5° beyond the beak tip up to +125° laterally. Vertically, a small strip from -10° below to about +25° above the horizon activated the visual wulst. Although retinal ganglion cells had a much higher density around the fovea and along a strip extending from the fovea towards the beak tip, these areas were not overrepresented in the wulst map. The wulst area activated from the foveal region of the ipsilateral eye, overlapped substantially with the middle of the three contralaterally activated regions in the visual wulst, and partially with the other two. Visual wulst activity evoked by stimulation of the frontal visual field was stronger with contralateral than with binocular stimulation. This confirms earlier electrophysiological studies indicating an inhibitory influence of the activation of the ipsilateral eye on wulst activity elicited by stimulating the contralateral eye. The lack of a foveal overrepresentation suggests that identification of objects may not be the primary task of the zebra finch visual wulst. Instead, this brain area may be involved in the processing of visual information necessary for spatial orientation.

No MeSH data available.


Related in: MedlinePlus