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Volume 27, Issue 14, Pages e5 (July 2017)

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1 Volume 27, Issue 14, Pages 2053-2064.e5 (July 2017)
Space-Specific Deficits in Visual Orientation Discrimination Caused by Lesions in the Midbrain Stimulus Selection Network  Eric I. Knudsen, Jason S. Schwarz, Phyllis F. Knudsen, Devarajan Sridharan  Current Biology  Volume 27, Issue 14, Pages e5 (July 2017) DOI: /j.cub Copyright © 2017 The Author(s) Terms and Conditions

2 Figure 1 Orientation Discrimination Task and Spatial Patterns of Peck Responses (A) The sequence of stimuli for the single-location and mirror-locations protocols are shown as a time series from left to right. The chicken was rewarded with brief access to food for pecking within 15° of the box following the horizontal grating (red arrow) or of the cross following the vertical grating (blue arrow). The visual stimuli and locations are not drawn to scale. (B) The spatial pattern of peck responses on the touch-sensitive computer screen for a single test session from C72 before an Ipc lesion (baseline). Responses to the horizontal grating are shown in red, and responses to the vertical grating are shown in blue. The locations of the grating, response box, and cross on the screen are indicated. This bird was tested with the mirror-locations protocol (STAR Methods), in which two grating locations at mirror-symmetrical positions (circled plaids at left and right 58°, 0° elevation) were randomly interleaved. The dashed line indicating the boundary used to define box responses and cross responses was drawn perpendicular to the line connecting the cross to the box (solid line). The d’ values for this particular test session are indicated. (C) Peck responses recorded on day 1 after the Ipc lesion. The lesioned (right) and non-lesioned (left) locations (at left and right 39°, 0° elevation) were tested on randomly interleaved trials. (D) Grating surrounded by distractors, used to test birds in group 2. The contrast of the four distractor dots was varied randomly across trials. See also Figure S1. Current Biology  , e5DOI: ( /j.cub ) Copyright © 2017 The Author(s) Terms and Conditions

3 Figure 2 Histological Reconstructions of Ipc Lesion Sites
(A) Lesion sites in group 1 birds. Transverse sections through the Ipc stained for cell bodies with cresyl violet (left) or for choline acetyl transferase (ChaT), the synthetic enzyme for the neurotransmitter acetylcholine. Note the intense somatic ChaT staining in the Ipc. Arrows indicate lesion sites. Important nuclei in the midbrain selection network are labeled in the left panel. OT, optic tectum; Ipc, nucleus isthmi pars parvocellularis; Imc, nucleus isthmi pars magnocellularis; SLu, nucleus isthmi pars semilunaris. (B) Lateral view of the chicken brain. Dashed lines, the percentage rostrocaudal locations of the transverse sections shown in (A) and (C). (C) Lesion sites (arrows) in group 2 birds. Scale bar is the same for all sections. Current Biology  , e5DOI: ( /j.cub ) Copyright © 2017 The Author(s) Terms and Conditions

4 Figure 3 Orientation Discrimination Performance before and after an Ipc Lesion (A and B) Data for group 1 birds. Performance measured at baseline (before the Ipc lesion; gray and white bars), at the Ipc-lesioned location (exptl loc; black bar), and at a non-lesioned location (cntrol loc; stippled bar). C70 and C76 were tested with the single-location protocol, and C72 was tested with the mirror-locations protocol (STAR Methods). The post-lesion data for the lesioned and non-lesioned locations were collected on the same day. The post-lesion data for C72 and C76 were collected on day 1 and for C70 on day 6, following the lesion. Number inside each bar is the sample size. (A) Percentage correct performance. (B) Discrimination accuracy (d’) (STAR Methods). ∗p < 0.05 and ∗∗p < 0.01, randomization test comparing pre-lesion with post-lesion responses. (C) Comparison of d’ measured before (Pre) and immediately after (Post) Ipc lesions for all birds (symbol key). (D and E) Data for group 2 birds. The birds were tested with the distractor protocol (STAR Methods). Post-lesion data were collected from C59 on day 4 and from C69 on day 1 for weak distractors and day 2 for strong distractors. (D) Percentage correct performance. (E) Discrimination accuracy. Gray and black bars, lesioned location (exptl loc); white and stippled bars, non-lesioned location (cntrol loc); bars without hatching, performance with weak distractors; bars with hatching, performance with strong distractors (defined in Figure S1). (F and G) Recovery of orientation discrimination following the Ipc lesion for all birds. (F) Percentage correct performance. (G) Discrimination accuracy (d’). The data represent responses to target gratings presented at the lesioned location plotted as a function of days following the Ipc lesion in each bird. The data from each bird are plotted with a distinct symbol (symbol key) and connected by a line. Open symbols, tested with weak or no distractors; filled symbols, strong distractors. See also Figure S2. Current Biology  , e5DOI: ( /j.cub ) Copyright © 2017 The Author(s) Terms and Conditions

5 Figure 4 Histological Reconstructions of OT Lesion Sites
(A) Lateral view of the chicken brain showing the plane of section and a cresyl violet-stained transverse section through the center of the OT lesion in C59. Numbers on the left identify the OT layers. (B) OT lesions in the group 1 birds, C70, C72, and C76. Camera lucida drawings show cresyl violet-stained transverse sections. The dark shading indicates the extent of overt scarring. Dashed line, layer 10; dotted line, layer 13. The percentage rostrocaudal location of each section is defined in (A). (C) OT lesions in the group 2 birds, C59 and C69. Current Biology  , e5DOI: ( /j.cub ) Copyright © 2017 The Author(s) Terms and Conditions

6 Figure 5 Spatial Patterns of Peck Responses before and after an OT Lesion Peck responses of C72 from single sessions, before and on day 1 following the OT lesion. The data are plotted as described in Figure 1B. Responses to the horizontal grating are shown in red, and responses to the vertical grating are shown in blue. The d’ values for these particular test sessions are indicated. (A) Baseline session before the OT lesion. Responses to the targets at left and right 63°, up 22° are shown on the left and right, respectively. (B) Peck responses recorded on day 1 after the OT lesion. The lesioned (right) and non-lesioned (left) locations were tested on randomly interleaved trials. Current Biology  , e5DOI: ( /j.cub ) Copyright © 2017 The Author(s) Terms and Conditions

7 Figure 6 Orientation Discrimination Performance before and after an OT Lesion (A–C) Data for group 1 birds are presented as described in Figure 3. The data represent performance only on trials with weak or no distractors. (A) Percent correct performance. (B) Discrimination accuracy. (C) Comparison of d’ before (Pre) and during the first week after (Post) the OT lesions for all birds (symbol key). C70 and C76 were tested with the single-location protocol, and C72 was tested with the distractor protocol (STAR Methods). (D and E) Data for the group 2 birds measured during week 1 (C69) or week 2 (C59) following the OT lesion are presented as described in Figure 3. (D) Percent correct performance. (E) Discrimination accuracy. The birds were tested with the cued-location protocol (STAR Methods), but the data were combined across cueing conditions. n.t., not tested. (F and G) Time course of orientation discrimination performance following the OT lesion. The data were combined across days of testing according to the week post-lesion when they were collected. (F) Percentage correct performance. (G) Discrimination accuracy (d’). The data represent responses to target gratings presented at the lesioned location plotted as a function of weeks (data combined across days of testing) following the OT lesion for each bird. The data from each bird are plotted with a distinct symbol (symbol key) and are connected by a line. Open symbols, tested with weak or no distractors; filled symbols, tested with strong distractors. See also Figures S1 and S3. Current Biology  , e5DOI: ( /j.cub ) Copyright © 2017 The Author(s) Terms and Conditions

8 Figure 7 Spatially Cued Orientation Discrimination Task
(A) The sequence of stimuli for the cued-location protocol (STAR Methods; Movie S1) is shown as a time series from left to right; only one of the multiple interleaved target conditions is shown. Either a valid spatial cue (red circle, top) or a neutral spatial cue (two green circles, bottom) preceded the stimulus sequence: left-right mirror-symmetric locations tested on interleaved trials, with the contrast of the four distractor dots varied randomly across trials. For the illustrated condition (horizontal grating), the correct response is to the box in both cases (red arrows). The visual stimuli and locations are not drawn to scale. (B) Data for the group 2 birds (C59 and C69) tested with the cued-location protocol before the OT lesion, ≤5 weeks post-lesion, and >5 weeks post-lesion. The bars indicate the difference in percentage correct measured for valid versus neutrally cued trials at the lesioned location (exptl loc) and non-lesioned location (cntrol loc). Data were combined across distractor strengths (∗p < 0.05 and ∗∗p < 0.01, Fisher’s exact test). Pre-lesion, C59 exhibited a cueing benefit only for targets on the right side (exptl loc: p = 0.019, n = 195 trials). Following the OT lesion, the cueing benefit was reduced dramatically ≤5 weeks post-lesion (p > 0.9, n = 64 trials). A benefit from cueing was marginal, but not significant, at the lesioned location (exptl loc) >5 weeks post-lesion (p > 0.1, n = 294 trials; weeks 6–11 post-lesion). No benefit appeared at the non-lesioned location (cntrol loc) during this period (p > 0.7, n = 294 trials; weeks 6–11 post-lesion). Pre-lesion, C69 exhibited improved discrimination performance on both sides with cueing (exptl loc [left]: p = 0.037, n = 712 trials; cntrol loc [right]: p = 0.028, n = 712 trials). Cueing had a detrimental effect on performance at the lesioned (exptl) location (p = 0.003, n = 825 trials; weeks 1–5 post-lesion), while continuing to benefit performance at the cntrol location (p = 0.015, n = 825 trials; weeks 1–5 post-lesion). No benefit from cueing appeared at the lesioned (exptl) location up to 12 weeks post-lesion (p > 0.5, n = 679 trials; weeks 6–12 post-lesion), while the benefit from cueing continued at the non-lesioned (cntrol) location throughout this period (p = 0.021, n = 688 trials; weeks 6–12 post-lesion). Current Biology  , e5DOI: ( /j.cub ) Copyright © 2017 The Author(s) Terms and Conditions


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