Influence of ocular dominance columns and patchy callosal connections on binocularity in lateral striate cortex: Long Evans versus albino rats

Abstract

In albino rats, it has been reported that lateral striate cortex (V1) is highly binocular, and that input from the ipsilateral eye to this region comes through the callosum. In contrast, in Long Evans rats, this region is nearly exclusively dominated by the contralateral eye even though it is richly innervated by the callosum (Laing, Turecek, Takahata, & Olavarria, 2015). We hypothesized that the inability of callosal connections to relay ipsilateral eye input to lateral V1 in Long Evans rats is a consequence of the existence of ocular dominance columns (ODCs), and of callosal patches in register with ipsilateral ODCs in the binocular region of V1 (Laing et al., 2015). We therefore predicted that in albino rats input from both eyes intermix in the binocular region, without segregating into ODCs, and that callosal connections are not patchy. Confirming our predictions, we found that inputs from both eyes, studied with the transneuronal tracer WGA-HRP, are intermixed in the binocular zone of albinos, without segregating into ODCs. Similarly, we found that callosal connections in albino rats are not patchy but instead are distributed homogeneously throughout the callosal region in V1. We propose that these changes allow the transcallosal passage of ipsilateral eye input to lateral striate cortex, increasing its binocularity. Thus, the binocular region in V1 of albino rats includes lateral striate cortex, being therefore about 25% larger in area than the binocular region in Long Evans rats. Our findings provide insight on the role of callosal connections in generating binocular cells.

Keywords: RRID:RGD_68073; Sprague-Dowley rat (RRID:RGD_70508); V1; columnar organization; eye-specific domains; interhemispheric connections; primary visual cortex.

Figure 1

WGA-HRP labeling of retino-dLGN-V1 projections in Long Evans and albino rats. (a) Representative case of Long Evans ipsilateral eye labeling (adapted from Laing et al., 2015). Note the distinct labeled patches in the central segment of V1 (outlined by white segmented line). (b) Representative case of ipsilateral eye WGA-HRP labeling in V1 of albino rat. Note that the labeling is more widespread than in Long Evans rats. The black line indicates the border of V1 determined based on the myelin pattern from the same case shown in (e) (see Materials and Methods). (c) The same case as in (b); the white segmented line delineates the WGA-labeled region in the central segment (see Materials and Methods). (d) Labeling in V1 contralateral to the eye injected with WGA-HRP for the albino case shown in (b). (e) Myelin pattern of V1 for albino case shown in (b). The border of V1 based on the myelin pattern is indicated by a black line (see Materials and Methods). (f) Plots of normalized mediolateral density profiles at the levels indicated in (b) and (e) show that the density of WGA-HRP labeling (black trace) declines more medially than that for the myelin pattern (grey trace), leaving a gap, about 0.20 mm in width, in lateral V1 of albino rats. (g) Labeling pattern in dLGN (top) and superior colliculus (SC, bottom) of Long Evans rat in (a). (h) Labeling pattern in dLGN and SC for albino case in (b). (i) Higher magnification of the dLGNs from the Long Evans and albino rats shown in (g), (h), respectively. Arrows indicate dorsomedial region that remains unlabeled after intraocular injections of WGA-HRP into the ipsilateral eye in both rat strains. This dLGN region innervates lateral V1 (see Refs. in text). Scale bars in (a), (g) and (i) = 1.0 mm. In (a) and (c), M = medial segment; C = central segment; L = lateral segment.

Figure 2

WGA-HRP labeling patterns and 3D surface plots for Long Evans and albino rats. (a) and (b) Two cases of Long Evans rats (top, adapted from Laing et al., 2015) and respective 3D surface plot reconstructions of the labeling pattern (bottom). (c), (d) Two cases of albino rats (top) and respective 3D surface plot reconstructions of labeling patterns. The 3D plots derive from the areas delineated with dashed lines in the top row. Scale bar = 1.0 mm. (e), (f) Patch Index: Area Method and SD Method for ODCs. (e) Average values of Patch Index Area method. Long Evans rats (n= 9) are significantly different from albino group (n = 7) (p = 0.002). (f) Average Patch Index Standard Deviation method. Long Evans rats (n = 9) are significantly different from the albino group (n = 7) (p = 0.001). Error bars in both graphs denote SEM for each group.

Figure 3

Callosal labeling in Long Evans and albino rats. (a), (b) Two examples of HRP- labeled callosal patterns in Long Evans rats (top, adapted from Laing et al. 2015) and respective 3D surface plot reconstructions (bottom). (c), (d) Two examples of HRP-labeled callosal patterns in albino rats (top) and respective 3D surface plot reconstructions of these cases (bottom). The white lines in the top row indicates the border between striate (V1) and lateral extrastriate cortex. Note that the 3D plots are reconstructed from both the CS and LS. Bright yellow indicates high labeling density; black indicates background. Scale bar = 1.0 mm. (e), (f) Patch Index: Area Method and SD Method for callosal connections. (e) Average values of Patch Index Area method for Long Evans (n = 8) and albino (n = 8) rats. Long Evans rats are significantly different from albino group (p = 0.032). (f) Average values of Patch Index Standard Deviation method for Long Evans (n =8) and albino (n = 8) rats. Long Evans rats are significantly different from the albino group (p = 0.017). Error bars in both graphs denote SEM for each group.

Figure 4

Recording sites in area V1 of albino rat. Callosotomy in albino rats. (a) Tangential section from callosotomized albino rat showing myelin pattern for V1 (arrows indicate the border of V1). Electrode penetrations (black dots) can be seen across V1. (b) Same section as in (a) showing border of V1 (black outline) and several additional electrode penetrations from same case in (a) identified after reconstruction from neighboring sections. The CS is outlined by white dashed line. This border was estimated using the information from cases analyzed as illustrated in Fig. 1 (see Materials and Methods). M = MS, C = CS, L = LS. (c) Coronal sections show transection of splenium of corpus callosum (arrows) in the top (anterior) two sections. The posterior section, at the level of the superior colliculus, demonstrates that the transection of splenium was complete. The left cortical mantle was removed for flattening and tangential sectioning. Scale bars = 1.0 mm. SC = Superior Colliculus; LGN = Lateral Geniculate Nucleus. (d), (e), (f) Quantitative analysis of binocularity in central and lateral segments of V1 in Long Evans and albino rats. (d) Central Segment. In albino rats, callosotomy shifts the ocular dominance preference from highly binocular (CBI = 0.11, n = 19 recording sites) to dominated by the contralateral eye (CBI = 0.52, n = 25 recording sites). In Long Evans rats, the contralateral eye exerts some dominance (CBI = 0.33, n = 33 recording sites), but not as strongly as in the LS (b). (e) Lateral Segment. Evoked responses were highly binocular in intact albino rats (CBI=0.16, n = 10 recording sites). After callosotomy, dominance by the contralateral eye increased significantly (CBI = 0.82, n = 11 recording sites), reaching a score similar to that of Long Evans rats in the LS (CBI= 0.74, n = 5 recording sites). This shift is greater than that observed in the CS region of albino rats (d). (f) Pooling of data from the central and lateral segments. Long Evans (n = 38 recording sites), intact albino rats (n = 29 recording sites) and callosotomized albino rats (n = 36 recording sites).

Figure 5

Influence of ODCs and patchy callosal connections on binocularity in the lateral segment of V1 (area 17). In both Long Evans and albino rats, callosal connections connect asymmetric, but topographically corresponding, loci in V1, such that opposite central and lateral segments connect reciprocally with each other (Lewis and Olavarria, 1995). (a) In Long Evans rats, ODCs and patchy callosal connections prevent the passage of ipsilateral eye input to the lateral segment. The left lateral segment (blue) cannot receive transcallosal input from the left, ipsilateral nasal retina (yellow) because the contralaterally dominated territory in the right central segment (yellow) is deprived of callosal connections (callosal patches correlate with ipsilateral ODCs, colored blue, Laing et al., 2015). (b) In contrast, we found that albino rats lack ODCs and patchy callosal connections. Thalamic inputs from right and left eyes are intermixed in the central segment (blue + yellow = green), allowing the callosal pathway to convey input from the ipsilateral eye to the lateral segment in the left hemisphere, thereby increasing binocularity in this segment (green). The same explanation applies to the right LS, not drawn for simplicity. M: medial segment, C: central segment, L: lateral segment.