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Showing content from https://pubmed.ncbi.nlm.nih.gov/26691828/ below:

Thalamic nuclei convey diverse contextual information to layer 1 of visual cortex

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. 2016 Feb;19(2):299-307. doi: 10.1038/nn.4197. Epub 2015 Dec 21. Thalamic nuclei convey diverse contextual information to layer 1 of visual cortex

Affiliations

¹ Biozentrum, University of Basel, Switzerland.
² Department of Neuroscience, Physiology and Pharmacology, University College London, London, UK.

PMID: 26691828
PMCID: PMC5480596
DOI: 10.1038/nn.4197

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Thalamic nuclei convey diverse contextual information to layer 1 of visual cortex

Morgane M Roth et al. Nat Neurosci. 2016 Feb.

. 2016 Feb;19(2):299-307. doi: 10.1038/nn.4197. Epub 2015 Dec 21. Affiliations

¹ Biozentrum, University of Basel, Switzerland.
² Department of Neuroscience, Physiology and Pharmacology, University College London, London, UK.

PMID: 26691828
PMCID: PMC5480596
DOI: 10.1038/nn.4197

Item in Clipboard

Abstract

Sensory perception depends on the context in which a stimulus occurs. Prevailing models emphasize cortical feedback as the source of contextual modulation. However, higher order thalamic nuclei, such as the pulvinar, interconnect with many cortical and subcortical areas, suggesting a role for the thalamus in providing sensory and behavioral context. Yet the nature of the signals conveyed to cortex by higher order thalamus remains poorly understood. Here we use axonal calcium imaging to measure information provided to visual cortex by the pulvinar equivalent in mice, the lateral posterior nucleus (LP), as well as the dorsolateral geniculate nucleus (dLGN). We found that dLGN conveys retinotopically precise visual signals, while LP provides distributed information from the visual scene. Both LP and dLGN projections carry locomotion signals. However, while dLGN inputs often respond to positive combinations of running and visual flow speed, LP signals discrepancies between self-generated and external visual motion. This higher order thalamic nucleus therefore conveys diverse contextual signals that inform visual cortex about visual scene changes not predicted by the animal's own actions.

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Conflict of interest statement

The authors declare no competing financial interests.

Figures
Figure 1. Connectivity of the lateral posterior…

Figure 1. Connectivity of the lateral posterior nucleus (LP)

( a ) Projections to LP.…

Figure 1. Connectivity of the lateral posterior nucleus (LP)

(a) Projections to LP. Retrograde tracer injection into LP (CTB; insets in top panel: left, schematic of the injection; right, injection site) and areas with substantial numbers of retrogradely labelled cell bodies. Top: V1, primary visual cortex; Hip, hippocampus; SC, superior colliculus; TEa, temporal association area; VisM, medial visual areas; VisL, lateral visual areas; Bottom: ACAd, dorsal anterior cingulate cortex; ACAv, ventral anterior cingulate cortex; MO2, secondary motor area; PPC, posterior parietal cortex; SC: superior colliculus, SuG, superficial gray layer; Op, optic layer; InG, intermediate gray layer. Arrows indicate the orientation of the coronal sections (similar for all images in this figure; M: medial; D: dorsal). (b) Organization of thalamic neurons projecting to V1 in coronal slices. Top, left panel: three retrograde tracer injections in V1 (see inset in bottom left corner; CTB488, CTB647 and CTB555) at different retinotopic locations. Retrogradely labelled neurons in dLGN (top, right panel) and in LP at two positions along the anterior-posterior axis (bottom panels). (c) Projections from LP and dLGN. Double injection of AAV2.1-Ef1a-eGFP into dLGN and AAV2.1-Ef1a-tdTomato into LP (left panels) and pattern of dLGN (green) and LP (magenta) axons in V1 (middle panels with an enlarged inset of layer 1). Right panel: normalized fluorescence intensity of LP (magenta) and dLGN axons (green) at different cortical depths in layer 1. Shaded areas denote s.e.m. Dots: weighted median of maximum fluorescence for individual brain slices. Black lines show the median, P = 0.03, Wilcoxon rank-sum test, n = 5 slices, 2 mice. Observations in a and b were reproduced in 11 and 3 mice, respectively.

Figure 2. Orientation and direction selectivity of…

Figure 2. Orientation and direction selectivity of thalamic input to V1.

( a ) Left,…

Figure 2. Orientation and direction selectivity of thalamic input to V1.

(a) Left, experimental schematic. Imaging responses of thalamo-cortical projections in V1 to drifting square-wave gratings using two-photon microscopy in anaesthetized mice expressing the calcium indicator GCaMP6 in dLGN. Middle, two-photon image of dLGN axons and putative axonal boutons in L1 of V1. Right, example fluorescence traces in response to 12 randomly interleaved grating directions (grey: eight individual repetitions re-ordered according to grating direction, black: average) and polar plots from two dLGN boutons (indicated by arrows; top bouton, OSI = 0.21, DSI = 0.13; bottom bouton: 0.91, 0.2). (b) Example responses of thalamo-cortical axonal boutons in L1 of V1 after GCaMP6 expression in the LP. Same layout as in a. (top bouton, OSI = 0.29, DSI = 0.38; bottom bouton: 0.81, 0.09) (c) Example responses of V1 layer 2/3 neurons. Same layout as in a. (top neuron, OSI = 0.95, DSI = 0.09; bottom neuron: 0.93, 0.91). (d,e) Distribution of orientation selectivity indices (OSIs, d) and direction selectivity indices (DSIs, e) of visually-responsive dLGN boutons, LP boutons and V1 cell bodies. Triangles indicate medians. *, p < 0.05; ***, p < 10⁻⁸, Wilcoxon rank-sum test. dLGN: n = 429 boutons, 6 mice, LP: n = 202 boutons, 6 mice, V1: n = 114 cells, 4 mice. All scale bars, 2 ΔF/F, 2 s.

Figure 3. Spatial receptive field properties of…

Figure 3. Spatial receptive field properties of thalamic input to V1.

( a ) Schematic…

Figure 3. Spatial receptive field properties of thalamic input to V1.

(a) Schematic of receptive field mapping stimuli: black and white squares (8 deg x 8 deg) on a gray background. (b) Responses of an ON-selective dLGN bouton to white squares (top) and an OFF-selective LP bouton to black squares (bottom) at different positions. Left, two-photon image of dLGN (top) and LP (bottom) projections in L1 of V1. Middle left, example fluorescence traces of a single bouton (indicated by arrows; individual traces in gray, averages in black) ordered according to stimulus position. Scale bars, 400% ΔF/F, 2 s. Middle right, receptive fields of the boutons. Far right, smoothed receptive fields. Line indicates receptive field outline (see Methods). (c,d) Distributions of spatial receptive field size (c), and the ratio of major to minor axis length of receptive fields (d) of dLGN and LP boutons and V1 layer 2/3 cell bodies. Triangles indicate medians. ***, P < 10⁻¹⁰, Wilcoxon rank-sum test. dLGN: n = 2317 receptive fields, 7 mice, LP: 1825 receptive fields, 13 mice, V1: 356 receptive fields, 4 mice.

Figure 4. Scatter and visual field coverage…

Figure 4. Scatter and visual field coverage of thalamic spatial receptive fields.

( a )…

Figure 4. Scatter and visual field coverage of thalamic spatial receptive fields.

(a) Example population of all dLGN receptive fields from one 120 µm by 120 µm region in L1 of V1. Top, receptive field subdomains of individual boutons plotted at the boutons’ cortical x-y position within the imaged region. Bottom left, positions of subdomain centroids in visual space from the dLGN receptive fields above. Bottom right, sum of all dLGN receptive fields above, illustrating their visual field coverage. (b) All LP receptive field subdomains from an example region. Same layout as a. (c) Population of V1 layer 2/3 neuron receptive field subdomains from an example 250 µm by 250 µm region. Same layout as a except that the bottom panels refer to a 120 µm by 120 µm subset of the imaged region above (indicated by dashed-line square). (d) Distribution of receptive field scatter, determined by the distances between the centroids of pairs of receptive fields. For neurons or boutons with both ON and OFF subdomains, these were included separately (see Methods). dLGN: n = 273353, LP: n = 87804, V1: n = 1380 pairs of receptive fields. Triangles indicate medians. ***, p < 10⁻¹⁰, Wilcoxon rank-sum test. (e) Cumulative area covered by the population receptive field as a function of the number of individual receptive fields. Thin lines indicate individual imaged regions, thick lines indicate medians. dLGN: n = 20 regions, 7 mice, LP: n = 33 regions, 13 mice, V1: n = 8 regions (subdivided into 32), 4 mice.

Figure 5. Responses of LP and dLGN…

Figure 5. Responses of LP and dLGN boutons to eye movements.

( a ) Schematic…

Figure 5. Responses of LP and dLGN boutons to eye movements.

(a) Schematic of the virtual reality setup. (b) Calcium trace and inferred firing rate of an example bouton aligned to horizontal pupil position of the contralateral eye. Top left: images of the eye taken before and after a saccade. Red dashed lines indicate occurrences of saccades. Pupil position and inferred firing rate in arbitrary units. (c) Left: average traces of inferred firing rate (a.u.) of LP and dLGN boutons showing significantly increased activity in response to a saccade, aligned to saccade onset (dashed line) in the virtual environment (VR) and in the dark. Right: mean fraction of LP and dLGN boutons significantly modulated by saccades. Error bars are s.e.m. *, p < 0.05, Wilcoxon rank-sum test. VR dLGN, n = 21 sessions ; VR LP, n = 31 sessions; Dark dLGN, n = 21 sessions; Dark LP, n = 30 sessions; LP, 10 mice; dLGN: 8 mice.

Figure 6. LP and dLGN carry distinct…

Figure 6. LP and dLGN carry distinct visual, motor and visuo-motor signals.

( a,b )…

Figure 6. LP and dLGN carry distinct visual, motor and visuo-motor signals.

(a,b) Left: calcium traces of two example boutons aligned to visual flow speed (VF) of the virtual corridor (a, yellow) or the running speed (RS) of the animal (b, blue) in the open-loop condition of the virtual reality (virtual visual flow speed uncoupled from running speed). Right, virtual visual flow speed (a) and running speed (b) tuning curves for example boutons. Lines above tuning curves indicate significant bins (see Methods). Error bars are s.e.m. (c) Top: example traces of RS and VF, over-plotted with model predictions for these traces (gray traces) from a random forest decoder trained with inferred spikes from single example boutons (see Methods). PP: prediction power between observed variable and single-bouton prediction over the whole recording. Bottom: proportions of dLGN and LP boutons conveying significant information (PP > 0.16) about RS or VF. (d) Relationship between the ‘signed’ prediction power (PP) for RS and for VF for all boutons. A sign was assigned to each PP according to the sign of the linear correlation coefficient between activity and RS or VF for each bouton (see Methods). Only boutons with |PP| > 0.16 from the origin (colored points in scatter plots) were included in the analysis in e and f. (e) Circular histogram showing the distribution of LP and dLGN boutons with different interaction angles θ between the ‘signed’ PP for RS and VF (see manuscript text and Methods). (f) Left: tuning curves for RS and VF for two example boutons. Top left: anticorrelated tuning curves typical of boutons with θ ~135° (R, Pearson’s correlation coefficient). Bottom left: correlated tuning curves typical of boutons with θ ~45°. Right: distributions of correlation coefficients R between RS and VF tuning curves (TCs) of individual boutons. ***, P < 10⁻⁷, Wilcoxon rank-sum test. dLGN: n = 2159 boutons, 8 mice, LP: n = 1617 boutons, 10 mice.

Figure 7. Visuo-motor discrepancy signals are enriched…

Figure 7. Visuo-motor discrepancy signals are enriched in LP.

( a ) Calcium traces and…

Figure 7. Visuo-motor discrepancy signals are enriched in LP.

(a) Calcium traces and inferred firing rate (top) of two example boutons aligned to the difference between running speed and visual flow speed (RS–VF, left) or the equal sum of RS and VF (RS+VF, right), over-plotted with model predictions for these traces (gray) obtained with a random forest decoder trained on inferred spike rates from the example boutons above. PP: prediction power. Bottom: aligned running speed and visual flow speed traces. Gray shaded regions reflect periods of elevated RS−VF or RS+VF (horizontal black lines indicate zero). (b) Example imaged regions. Boutons with highest PP for RS, VF, RS–VF or RS+VF are indicated by different colors (if PP > 0.16). (c) Circular histogram with distributions of interaction angles θ for different groups of LP and dLGN boutons. Similar to Fig.6e, but boutons were grouped according to which variable they predicted best (groups with highest PP for RS, VF, RS+VF or RS−VF are indicated by different colors). (d) Proportions of dLGN and LP boutons with highest PP for RS−VF or RS+VF (if PP > 0.16) out of all boutons. Wilcoxon rank-sum test. dLGN: n = 18 regions, 8 mice, LP: n = 31 regions, 10 mice. (e) Average change in activity in the closed-loop condition relative to the open-loop condition for boutons most informative about RS–VF or RS+VF in the open-loop condition (thresholded average ΔF/F, see Methods; Wilcoxon signed-rank test; dLGN: RS+VF, 334 boutons, RS–VF, 206 boutons, n = 10 session pairs, 7 mice, LP: RS+VF, 99 boutons, RS–VF, 276 boutons, n = 13 session pairs, 8 mice.). **, P<0.01; ***, P<10⁻¹⁰.