Stefan Treue

In primates, primary visual cortex (V1) circuits support early visual processing, whereas in the lateral prefrontal cortex (LPFC), they support higher-order computations. Here, we characterized the intrinsic electrophysiological (e)-properties and morphology of excitatory (EXC), fast-spiking inhibitory (FSI), and non-fast-spiking inhibitory (NFSI) neurons in layers I-III of V1 and LPFC, of a small primate, the common marmoset. EXC and FSI neurons exhibited broader action potentials in LPFC than in V1. Compared to V1, LPFC EXC neurons exhibited reduced excitability, whereas FSI neurons showed increased excitability. NFSI neurons showed fewer area-specific differences. Notably, EXC and FSI neurons displayed increased bursting in LPFC compared to V1. Morphologically, LPFC-EXC neurons exhibited longer dendritic arbors, whereas LPFC-FSI neurons showed greater axonal complexity relative to V1. Our findings demonstrate area-specific functional and anatomical diversification of major neuronal types in layers I-III of the primate neocortex and provide an open-access resource for studies of neocortical cell types.

Perceptual processing may rhythmically alternate. There is a line of evidence from dense sampling psychophysics supporting this claim: In such studies, performance in visual target detection or discrimination is repeatedly tested at various fine-grained time intervals relative to a reference event. This reference event is presented at the beginning of each trial, and it is thought to reset some internal oscillation. Performance time courses following the reset often show rhythmic oscillations in the sub-second range. The interpretation has been that several quickly alternating peaks and troughs of perceptual efficiency exist. Here, we propose an alternative. Instead of being rhythmic, the perceptual processing efficiency time course might exhibit only a single peak in each trial. If the temporal location of this peak is constrained to co-occur with one of the peaks of the internal continuing oscillation, rhythmicity in overall performance time courses can be explained when performance is computed across many trials. Applying this perspective to three published datasets (N = 44, N = 34, N = 11) and running simulations, we confirm the possible existence of such phase-aligned peaks in perceptual efficiency. We show that foreperiod priming (behavioural advantage of repeating the same time interval between reference and target from one trial to the next) alternates across time. This is predicted if peaks in perceptual efficiency are consistently allocated to those time intervals that coincide with a peak in the underlying oscillation. Priming therefore works best at these intervals, which coincide with a peak in the underlying oscillation.

Preference tests help to determine how highly individuals value different options to choose from. During preference testing, two or more options are presented simultaneously, and options are ranked based on the choices made. Presented options, however, influence each other, where the amount of influence increases with the number of options. Multiple binary choice tests can reduce this degree of influence, but conventional analysis methods do not reveal the relative strengths of preference, i.e., the preference difference between options. Here, we demonstrate that multiple binary comparisons can be used not only to rank but also to scale preferences among many options (i.e., their worth value). We analyzed human image preference data with known valence scores to develop and validate our approach to determine how known valence ranges (high vs. low) converge on a scaled representation of preference data. Our approach allowed us to assess the valence of ranked options in mice and rhesus macaques. By conducting simulations, we developed an approach to incorporate additional option choices into existing rank orders without the need to conduct binary choice tests with all original options, thus reducing the number of animal experiments needed. Two quality measures, consensus error and intransitivity ratio, allow for assessing the achieved confidence of the scaled ranking and better tailoring of measurements required to improve it further. The software is available as an R package (“simsalRbim”). Our approach optimizes preference testing, e.g., in welfare assessment, and allows us to efficiently and quantitatively assess the relative value of options presented to animals.

Performing visually guided behavior involves flexible routing of sensory information towards associative areas. We hypothesize that in visual cortical areas, this routing is shaped by a gating influence of the local neuronal population on the activity of the same population's single neurons. We analyzed beta frequencies (representing local population activity), high-gamma frequencies (representative of the activity of local clusters of neurons), and the firing of single neurons in the medial temporal (MT) area of behaving rhesus monkeys. Our results show an influence of beta activity on single neurons, predictive of behavioral performance. Similarly, the temporal dependence of high-gamma on beta predicts behavioral performance. These demonstrate a unidirectional influence of network-level neural dynamics on single-neuron activity, preferentially routing relevant information. This demonstration of a local top-down influence unveils a previously unexplored perspective onto a core feature of cortical information processing: the selective transmission of sensory information to downstream areas based on behavioral relevance.

Spatial accuracy in electrophysiological investigations is paramount, as precise localization and reliable access to specific brain regions help the advancement of our understanding of the brain’s complex neural activity. Here, we introduce a novel, multi camera-based, frameless neuronavigation technique for precise, 3-dimensional electrode positioning in awake monkeys. The investigation of neural functions in awake primates often requires stable access to the brain with thin and delicate recording electrodes. This is usually realized by implanting a chronic recording chamber onto the skull of the animal that allows direct access to the dura. Most recording and positioning techniques utilize this implanted recording chamber as a holder of the microdrive or to hold a grid. This in turn reduces the degrees of freedom in positioning. To solve this problem, we require innovative, flexible, but precise tools for neuronal recordings. We instead mount the electrode microdrive above the animal on an arch, equipped with a series of translational and rotational micromanipulators, allowing movements in all axes. Here, the positioning is controlled by infrared cameras tracking the location of the microdrive and the monkey, allowing precise and flexible trajectories. To verify the accuracy of this technique, we created iron deposits in the tissue that could be detected by MRI. Our results demonstrate a remarkable precision with the confirmed physical location of these deposits averaging less than 0.5 mm from their planned position. Pilot electrophysiological recordings additionally demonstrate the accuracy and flexibility of this method. Our innovative approach could significantly enhance the accuracy and flexibility of neural recordings, potentially catalyzing further advancements in neuroscientific research.

Spatial attention represents a powerful top–down influence on sensory responses in primate visual cortical areas. The frontal eye field (FEF) has emerged as a key candidate area for the source of this modulation. However, it is unclear whether the FEF exerts its effects via its direct axonal projections to visual areas or indirectly through other brain areas and whether the FEF affects both the enhancement of attended and the suppression of unattended sensory responses. We used pathway-selective optogenetics in rhesus macaques performing a spatial attention task to inhibit the direct input from the FEF to area MT, an area along the dorsal visual pathway specialized for the processing of visual motion information. Our results show that the optogenetic inhibition of the FEF input specifically reduces attentional modulation in MT by about a third without affecting the neurons’ sensory response component. We find that the direct FEF-to-MT pathway contributes to both the enhanced processing of target stimuli and the suppression of distractors. The FEF, thus, selectively modulates firing rates in visual area MT, and it does so via its direct axonal projections.

Research on the psychological and physiological well-being of captive animals has focused on investigating different types of social and structural enrichment. Consequently, cognitive enrichment has been understudied, despite the promising external validity, comparability, and applicability. As we aim to fill this gap, we developed an interactive, multiple-choice interface for cage-mounted touchscreen devices that rhesus monkeys (Macaca mulatta) can freely interact with, from within their home enclosure at the Cognitive Neuroscience Laboratory of the German Primate Center. The multiple-choice interface offers interchangeable activities that animals can choose and switch between. We found that all 16 captive rhesus macaques tested consistently engaged with the multiple-choice interface across 6 weekly sessions, with 11 of them exhibiting clear task preferences, and displaying proficiency in performing the selected tasks. Our approach does not require social separation or dietary restriction and is intended to increase animals’ sense of competence and agency by providing them with more control over their environment. Thanks to the high level of automation, our multiple-choice interface can be easily incorporated as a standard cognitive enrichment practice across different facilities and institutes working with captive animals, particularly non-human primates. We believe that the multiple-choice interface is a sustainable, scalable, and pragmatic protocol for enhancing cognitive well-being and animal welfare in captivity.

Saccadic eye movements play a key role in gaining information about the surrounding environment. However, the neural mechanisms underlying the timing of these eye movements remain poorly understood. Here, we investigated the entrainment of saccadic eye movement by oscillatory neural activities in rhesus monkeys performing a visual foraging task. We found that saccades are phase-locked to beta LFP oscillations (16-22 Hz) in the frontal eye field (FEF), 100 ms before saccade onset, supporting a causal role of these oscillations in saccade timing. Furthermore, we show that the alignment between saccades and FEF LFPs varies, depending on the spatial relationship between the saccade target and the response field (RF) of neurons in the FEF. These findings suggest that the phase of the oscillatory neural activities determines the timing and direction of saccades.