Lukas Schneider’s research while affiliated with Leibniz Institute for Resilience Research and other places

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Publications (6)


Visual, delay, and oculomotor timing and tuning in macaque dorsal pulvinar during instructed and free choice memory saccades
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September 2023

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45 Reads

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4 Citations

Cerebral Cortex

Lukas Schneider

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Lydia Gibson

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Causal perturbations suggest that primate dorsal pulvinar plays a crucial role in target selection and saccade planning, though its basic neuronal properties remain unclear. Some functional aspects of dorsal pulvinar and interconnected frontoparietal areas—e.g. ipsilesional choice bias after inactivation—are similar. But it is unknown if dorsal pulvinar shares oculomotor properties of cortical circuitry, in particular delay and choice-related activity. We investigated such properties in macaque dorsal pulvinar during instructed and free-choice memory saccades. Most recorded units showed visual (12%), saccade-related (30%), or both types of responses (22%). Visual responses were primarily contralateral; diverse saccade-related responses were predominantly post-saccadic with a weak contralateral bias. Memory delay and pre-saccadic enhancement was infrequent (11–9%)—instead, activity was often suppressed during saccade planning (25%) and further during execution (15%). Surprisingly, only few units exhibited classical visuomotor patterns combining cue and continuous delay activity or pre-saccadic ramping; moreover, most spatially-selective neurons did not encode the upcoming decision during free-choice delay. Thus, in absence of a visible goal, the dorsal pulvinar has a limited role in prospective saccade planning, with patterns partially complementing its frontoparietal partners. Conversely, prevalent visual and post-saccadic responses imply its participation in integrating spatial goals with processing across saccades.

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Figure 3. Spatial tuning and response modulation per epoch. Spatial tuning and response modulation of all 322 units recorded during the memory-guided saccade task. The analyzed epochs are fixation hold (Fhol), cue onset (Cue), memory (Mem), pre-saccadic (Pre), Peri-saccadic (Peri), Post-saccadic (Post), target onset (Tons), and target hold (Thol). A: Total number of units (and percentages) showing response modulation relative to the respective baseline, for each analyzed epochs: no enhancement nor suppression (white), only suppression (blue), bidirectional -enhancement for one hemifield and suppression for the other (green), only enhancement (red). B: Number of units that, in the respective epoch, were not tuned (white), did not prefer either hemifield but showed a main effect of position in a one-way ANOVA (purple), preferred ipsilateral hemifield (orange), preferred contralateral hemifield (magenta). The patterns of response modulation and tuning were largely comparable across the two animals. The most noticeable difference between monkeys was that monkey C showed stronger contralateral cue preference (N=53) compared to ipsilateral cue preference (N=7) than monkey L (N=23 and N=11, respectively). See Supplementary Figure S1 for the relationship between response modulation and spatial tuning in each epoch.
Visual, delay and oculomotor timing and tuning in macaque dorsal pulvinar during instructed and free choice memory saccades

December 2021

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77 Reads

Causal perturbation studies suggest that the primate dorsal pulvinar (dPul) plays a crucial role in target selection and saccade planning, but many of its basic visuomotor neuronal properties are unclear. While some functional aspects of dPul and interconnected frontoparietal areas - such as ipsilesional choice bias after inactivation - are similar, it is not known if dPul neurons share oculomotor response properties of cortical circuitry. In particular, the delay period and choice-related activity have not been explored. Here we investigated visuomotor timing and tuning in macaque dPul during instructed and free choice memory saccades using electrophysiological recordings. Most units (80%) showed significant visual (16%), visuomotor (29%) or motor-related (35%) responses. Visual cue responses were mainly contralaterally-tuned; motor responses showed weak contralateral bias. Saccade-related responses (enhancement and suppression) were more common (64%) than cue-driven responses (45%). Pre-saccadic enhancement was less frequent (9-15% depending on the definition), and only few units exhibited classical visuomotor patterns such as a combination of cue and continuous delay period activity up to the saccade onset, or pre-saccadic ramping. Instead, activity was often suppressed during movement planning (30%) and execution phases (19%). Interestingly, most spatially-selective neurons did not encode the upcoming decision during the delay in free choice trials. Thus, in absence of a visible goal, the dorsal pulvinar has only a limited role in the prospective motor planning, with response patterns partially complementary to its frontoparietal cortical partners. Conversely, prevalent cue and post-saccadic responses imply that the dorsal pulvinar participates in integrating spatial goals with processing across saccades.


Fig. 3. Gaze dependence during initial fixation and recording sites. A: classification of initial gaze dependence. Data are normalized firing rates of each unit with a significant main effect of gaze on firing rates in the initial fixation epoch. Each line represents 1 unit. X-axis indicates initial gaze position: C, contralateral; S, straight ahead; I, ipsilateral. B: localization of recorded units in chamber-normal coronal sections in each monkey (monkey L and monkey C) and specific grid locations relative to the chamber center (x,y in parentheses). Locations were jittered along the horizontal dimension for better visualization. Black dashed lines indicate the projection of penetration tracks and mark the actual horizontal location of recorded neurons. Each circle represents 1 unit; colors indicate the initial gaze effects of the unit: orange for monotonic contralateral preference, red for monotonic ipsilateral preference, blue for central gaze preference, and green for nonmonotonic peripheral preference. Units that did not show a significant effect of gaze are shown in white. Pulvinar nuclei outlines (MPul/LPul/IPul, medial/ lateral/inferior pulvinar) were adapted from the NeuroMaps atlas (Rohlfing et al. 2012), exported via Scalable Brain Atlas, https://scalablebrainatlas.incf.org/macaque/ DB09 and https://scalablebrainatlas.incf. org/services/rgbslice.php (Bakker et al. 2015), and LPul was further subdivided into dorsal (PLdm) and ventral (PLvl) parts according to the brachium of the superior colliculus. See Supplemental Table S5 for data on individual monkeys.
Fig. 5. Dynamics of eye position signals across saccades. Population activity is plotted separately for neurons that shift from a low to high firing rate (POS; red) and for units shifting from a high to low firing rate (NEG; blue) across successive fixations. The derived eye position signal, obtained by subtracting NEG from POS (POS-NEG) is shown in green (see MATERIALS AND METHODS for details). Vertical lines indicate average onset of events across all trials: fixation point onset (FP onset), the monkey acquiring fixation (Fix), the cue onset (Cue), the cue offset and beginning of the memory period (Memory), the offset of the central fixation point (Go), the saccade onset (Saccade), the monkey acquiring the invisible target location (Sac end), the onset of the confirmation target (Tar Onset), and the end of the trial (Reward). Discontinuous traces indicate 2 different alignments to cue onset and saccade onset (purple lines). A: POS and NEG derived using the memory period for presaccadic fixation (Mem; gray-shaded box) and the target hold for postsaccadic fixation (Thol; gray-shaded box). Here, 131 units contributed to POS and 98 to NEG, and in total 153 units contributed to the eye position signal POS-NEG. On average, 21 1 units contributed to POS in each condition (i.e., a combination of initial and final gaze), 12 1 to NEG, and 33 2 to POS-NEG (means SE). B: magnified view of eye position signals around the saccade (black outline in A). Gray-shaded box indicates the duration of the saccade, and black dashed line indicates the timing of eye position scaled to match the step in firing rates. C and D: same as A and B, but using the initial fixation period (Fhol; gray-shaded box) for presaccadic fixation. Here, 124 units contributed to POS, 113 to NEG, and 153 to POS-NEG. On average, 17 1 units contributed to POS in each condition, 15 1 to NEG, and 32 2 to POS-NEG.
Patterns of final gaze dependence
Relationship between initial gaze effect and cue responses
Eye position signals in the dorsal pulvinar during fixation and goal-directed saccades

November 2019

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82 Reads

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19 Citations

Journal of Neurophysiology

Sensorimotor cortical areas contain eye position information thought to ensure perceptual stability across saccades and underlie spatial transformations supporting goal-directed actions. One pathway by which eye position signals could be relayed to and across cortical areas is via the dorsal pulvinar. Several studies demonstrated saccade-related activity in the dorsal pulvinar and we have recently shown that many neurons exhibit post-saccadic spatial preference. In addition, dorsal pulvinar lesions lead to gaze-holding deficits expressed as nystagmus or ipsilesional gaze bias, prompting us to investigate the effects of eye position. We tested three starting eye positions (-15°/0°/15°) in monkeys performing a visually-cued memory saccade task. We found two main types of gaze dependence. First, ~50% of neurons showed dependence on static gaze direction during initial and post-saccadic fixation, and might be signaling the position of the eyes in the orbit, or coding foveal targets in a head/body/world-centered reference frame. The population-derived eye position signal lagged behind the saccade. Second, many neurons showed a combination of eye-centered and gaze-dependent modulation of visual, memory and saccadic responses to a peripheral target. A small subset showed effects consistent with eye position-dependent gain modulation. Analysis of reference frames across task epochs from visual cue to post-saccadic fixation indicated a transition from predominantly eye-centered encoding to representation of final gaze or foveated locations in non-retinocentric coordinates. These results show that dorsal pulvinar neurons carry information about eye position, which could contribute to steady gaze during postural changes and to reference frame transformations for visually-guided eye and limb movements.


Eye position signals in the dorsal pulvinar during fixation and goal-directed saccades

July 2019

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39 Reads

Most sensorimotor cortical areas contain eye position information thought to ensure perceptual stability across saccades and underlie spatial transformations supporting goal-directed actions. One pathway by which eye position signals could be relayed to and across cortical areas is via the dorsal pulvinar. Several studies demonstrated saccade-related activity in the dorsal pulvinar and we have recently shown that many neurons exhibit post-saccadic spatial preference long after the saccade execution. In addition, dorsal pulvinar lesions lead to gaze-holding deficits expressed as nystagmus or ipsilesional gaze bias, prompting us to investigate the effects of eye position. We tested three starting eye positions (−15°/0°/15°) in monkeys performing a visually-cued memory saccade task. We found two main types of gaze dependence. First, ∼50% of neurons showed an effect of static gaze direction during initial and post-saccadic fixation. Eccentric gaze preference was more common than straight ahead. Some of these neurons were not visually-responsive and might be primarily signaling the position of the eyes in the orbit, or coding foveal targets in a head/body/world-centered reference frame. Second, many neurons showed a combination of eye-centered and gaze-dependent modulation of visual, memory and saccadic responses to a peripheral target. A small subset showed effects consistent with eye position-dependent gain modulation. Analysis of reference frames across task epochs from visual cue to post-saccadic target fixation indicated a transition from predominantly eye-centered encoding to representation of final gaze or foveated locations in non-retinocentric coordinates. These results show that dorsal pulvinar neurons carry information about eye position, which could contribute to steady gaze during postural changes and to reference frame transformations for visually-guided eye and limb movements. New & Noteworthy Work on the pulvinar focused on eye-centered visuospatial representations, but position of the eyes in the orbit is also an important factor that needs to be taken into account during spatial orienting and goal-directed reaching. Here we show that dorsal pulvinar neurons are influenced by eye position. Gaze direction modulated ongoing firing during stable fixation, as well as visual and saccade responses to peripheral targets, suggesting involvement of the dorsal pulvinar in spatial coordinate transformations.


Fig. 1 e Lesion reconstruction of patient M.B. Magnified views of fluid-attenuated inversion recovery (FLAIR) MR images of patient M.B. in MNI-space, co-registered to the digital version of the Morel atlas. Images were acquired in February 2016 when the behavioral testing took place. The top left shows a sagittal section indicating the orientation of the axial crosssections. FLAIR images show hyperintensity in the medial pulvinar on both sides, stronger in the left pulvinar (radiological convention with left hemisphere shown on the right side). Lesions spared the ventral pulvinar portions, anterior thalamus, brainstem, cerebellum and surrounding cortices. Cross-sections show the lesioned thalamic regions based on the overlaid pulvinar regions defined by the Morel atlas. Corresponding sections of the Morel atlas with all regions are shown on the right to the FLAIR images. The thalamic regions from the Morel atlas are outlined in light blue, except for medial pulvinar (PuM, red), lateral pulvinar (PuL, green), and anterior pulvinar (PuA, orange). A: anterior; CL: central lateral nucleus; L: left; MD: mediodorsal nucleus; P: posterior; R: right; VPL: ventral posterior lateral nucleus. x, z (in mm) denote the level of the cross-sections in MNI-space. 
Fig. 2 e Reach-grasp deficits of M.B. (A) Typical grasp postures. Healthy control (left) and M.B. (right). Left hand: note the abnormal wrist angle (red arrow) and the absence of a precision grip. Right hand: note the attempted precision grip with the right hand, but off the target (red arrow). Also note that the non-acting hand is not dystonic but is used to hold the collected objects. (B) Typical reach-grasp sequence of M.B. with the left hand under unconstrained viewing conditions. Note the abduction of the thumb, absence of a precision grip (red arrow) and scooping movement for picking up the object. (C) Typical reach-grasp sequence of M.B. with the right hand. Note that scaling of the grip was too wide at the contact with the table and the object was squeezed between the index finger and the base of the abducted thumb (red arrows). 
Fig. 3 e Reaching performance with foveal and extrafoveal viewing of the target. (A) Foveal reach task. (B) Extrafoveal reach task. (C,D) Endpoints of reaching movements in the foveal (left) and extrafoveal (right) reach tasks. Data are separated by visual hemifield (LVF and RVF) and hand (see Legend). Ellipses represent the horizontal and the vertical standard deviation over trials in M.B. and the mean standard deviation of the seven age-matched healthy control subjects. Note the larger endpoint variability in M.B. as compared to the healthy subjects, for reaches with both hands. (E,F) Absolute reaching inaccuracy (mean Euclidian distance from the reach target) for patient M.B. and controls as a function of hemifield, hand and reach task. Each dot represents the mean of a single subject, red connection lines indicate statistical significance of differences between M.B. and controls computed with the Crawford modified t-test, **p < .01. LVF: left visual hemifield, RVF: right visual hemifield. 
Fig. 4 e Reach latencies and durations in the foveal and extrafoveal reach task. (A,B) Reach latencies denoting the time between offset of the hand fixation spot and lift of the finger from the screen for correct trials, as a function of hand and hemifield, in the foveal (A) and extrafoveal (B) reach tasks. (C,D) Mean movement duration as a function of hand and hemifield in the foveal (C) and extrafoveal (D) reach tasks. Duration was computed from movement onset (lift of the finger from the touch screen) until target acquisition within the 5 success window around the target. In (AeD) each dot represents the mean of a single subject, red connection lines indicate statistical significance of differences between M.B. and the controls computed with the Crawford modified t-test, *p < .05, **p < .01, ***p < .001. LVF: left visual hemifield, RVF: right visual hemifield. 
Fig. 5 e Perceptual evidence accumulation performance. (A) Visual decision task with two alternative forced choices. (B) Psychometric curves of % rightward choices as a function of number of flickers presented to the right minus number of flickers to the left. Curves represent fitting of a four parameters sigmoid function, dots the unfitted raw percentages (purple: patient M.B., black: healthy controls). Note the similarity of the curves, indicating that M.B. was able to accumulate perceptual evidence from both sides of space and to form a correct decision. (C,D) Each dot represents the spatial bias defined as the inflection point of the sigmoidal curve (C), or the slope of each individual subject (D). Note that spatial bias and slope of M.B. were in the range of the healthy subjects. 
Reach and grasp deficits following damage to the dorsal pulvinar

November 2017

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413 Reads

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30 Citations

Cortex

Expansion of the dorsal pulvinar in humans and its anatomical connectivity suggests its involvement in higher-order cognitive and visuomotor functions. We investigated visuomotor performance in a 31 year old patient with a lesion centered on the medial portion of the dorsal pulvinar (left > right) due to an atypical Sarcoidosis manifestation. Unlike lesions with a vascular etiology, the lesion of M.B. did not include primary sensory or motor thalamic nuclei. Thus, this patient gave us the exceedingly rare opportunity to study the contribution of the dorsal pulvinar to visuomotor behavior in a human without confounding losses in primary sensory or motor domains. We investigated reaching, saccade and visual decision making performance. Patient data in each task was compared to at least seven age matched healthy controls. While saccades were hypometric towards both hemifields, the patient did not show any spatial choice or perceptual deficits. At the same time, he exhibited reach and grasp difficulties, which shared features with both, parietal and cerebellar damage. In particular, he had problems to form a precision grip and exhibited reach deficits expressed in decreased accuracy, delayed initiation and prolonged movement durations. Reach deficits were similar in foveal and extrafoveal viewing conditions and in both visual hemifields but were stronger with the right hand. These results suggest that dorsal pulvinar function in humans goes beyond its subscribed role in visual cognition and is critical for the programming of voluntary actions with the hands.


Table 1 . Summary of 56 stimulation datasets
Electrical Microstimulation of the Pulvinar Biases Saccade Choices and Reaction Times in a Time-Dependent Manner

January 2017

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66 Reads

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49 Citations

The Journal of Neuroscience : The Official Journal of the Society for Neuroscience

Significance statement: Despite a recent surge of interest, the core function of the pulvinar, the largest thalamic complex in primates, remains elusive. This understanding is crucial given the central role of the pulvinar in current theories of integrative brain functions supporting cognition and goal-directed behaviors, but electrophysiological and causal interference studies of dorsal pulvinar are rare. Building on our previous studies that pharmacologically suppressed dorsal pulvinar activity for several hours, here we used transient electrical microstimulation at different periods while monkeys performed instructed and choice eye movement tasks, to determine time-specific contributions of pulvinar to saccade generation and decision-making. We show that stimulation effects depend on timing and behavioral state, and that effects on choices can be dissociated from motor effects.

Citations (4)


... /2024 suppression following saccades, that initiated by the activation of inhibitory neurons in layer IV in area V4. The authors suggested the Pulvinar as a possible neural source for this response, which was previously suggested to carry CD signal from the SC to various visual areas such as MT in primates and V1 in rodents and primates (Stepniewska et al., 2000;Shipp, 2004;Berman and Wurtz, 2010;Kuang et al., 2012;Schneider et al., 2020Schneider et al., , 2023Miura and Scanziani, 2022). Therefore, the initial suppression phase we report can fit to a similar possible pathway from the SC through the Pulvinar into the inhibitory neurons in V1. ...

Reference:

The effect of microsaccades in the primary visual cortex: a two-phase modulation in the absence of visual stimulation
Visual, delay, and oculomotor timing and tuning in macaque dorsal pulvinar during instructed and free choice memory saccades

Cerebral Cortex

... In contrast, the dorsal pulvinar-comprising the PLdm and PM-aligns more with higher-order cognitive processes [21]. It is functionally connected to the frontal, parietal, and cingulate cortices and plays a critical role in attentional control, such as goal-directed eye movements, and other complex cognitive functions [26,37,55]. Particularly, the PM processes fear-eliciting stimuli, such as images of snakes, through its connections with the amygdala [45,[56][57][58][59]. ...

Eye position signals in the dorsal pulvinar during fixation and goal-directed saccades

Journal of Neurophysiology

... Thalamic connectivity with basal ganglia regions, including the putamen, pallidum, and caudate, remains consistent across tasks. In both tasks, all posterior group nuclei exhibit strong connectivity with basal ganglia regions, suggesting their involvement in voluntary movements and visual signal processing (Wilke et al., 2018, Cortes et al., 2024, Shimono et al., 2012. ...

Reach and grasp deficits following damage to the dorsal pulvinar

Cortex

... More ventral pulvinar regions, on the other hand, are functionally more connected with the ventral occipital and temporal cortex. This ventro-dorsal functional gradient of the pulvino-cortical functional connectivity is also in agreement with the literature ( Arcaro et al., 2015( Arcaro et al., , 2018Dominguez-Vargas et al., 2017;Shipp, 2003;Wilke et al., 2010). ...

Electrical Microstimulation of the Pulvinar Biases Saccade Choices and Reaction Times in a Time-Dependent Manner

The Journal of Neuroscience : The Official Journal of the Society for Neuroscience