Despite strong evidence to the contrary in the literature, microsaccades are overwhelmingly described as involuntary eye movements. Here we show in both human subjects and monkeys that individual microsaccades of any direction can easily be triggered: (1) on demand, based on an arbitrary instruction, (2) without any special training, (3) without visual guidance by a stimulus, and (4) in a spatially and temporally accurate manner. Subjects voluntarily generated instructed “memory-guided” microsaccades readily, and similarly to how they made normal visually-guided ones. In two monkeys, we also observed midbrain superior colliculus neurons that exhibit movement-related activity bursts exclusively for memory-guided microsaccades, but not for similarly-sized visually-guided movements. Our results demonstrate behavioral and neural evidence for voluntary control over individual microsaccades, supporting recently discovered functional contributions of individual microsaccade generation to visual performance alterations and covert visual selection, as well as observations that microsaccades optimize eye position during high acuity visually-guided behavior.

Graphical Abstract Highlights d We simulate ripples with two compartment models in a CA3-CA1 hippocampal network d Simulated ripples emerge in CA1 due to excitation paced by recurrent inhibition d They exhibit slow-gamma band CA3-CA1 coordination relayed by CA1 feedback inhibition d CA1 feedback inhibition is also key to control cell participation and sequence replay In Brief Hippocampus replays mnemonic representations during the so-called ripple oscillations. Ramirez-Villegas et al. show in a biophysically realistic model how the content and temporal organization of representations are coordinated by recurrent interactions between pyramidal and inhibitory neurons, as well as gamma oscillations. SUMMARYHippocampal ripple oscillations likely support reactivation of memory traces that manifest themselves as temporally organized spiking of sparse neuronal ensembles. However, the network mechanisms concurring to achieve this function are largely unknown. We designed a multi-compartmental model of the CA3-CA1 subfields to generate biophysically realistic ripple dynamics from the cellular level to local field potentials. Simulations broadly parallel in vivo observations and support that ripples emerge from CA1 pyramidal spiking paced by recurrent inhibition. In addition to ripple oscillations, key coordination mechanisms involve concomitant aspects of network activity. Recurrent synaptic interactions in CA1 exhibit slow-gamma band coherence with CA3 input, thus offering a way to coordinate CA1 activities with CA3 inducers. Moreover, CA1 feedback inhibition controls the content of spontaneous replay during CA1 ripples, forming new mnemonic representations through plasticity. These insights are consistent with slow-gamma interactions and interneuronal circuit plasticity observed in vivo, suggesting a multifaceted ripple-related replay phenomenon. EXPERIMENTAL MODEL AND SUBJECT DETAILSFour male rhesus monkeys (Macaca Mulatta), aged 5-9 years were used in this study. MRI-compatible head holders and chambers were made out of PEEK (polyether etherketone; TecaPEEK, Ensinger, Nufringen, Germany), and implanted stereotaxically on the cranium of four monkeys using standard clinical aseptic techniques. Implants were secured with custom-made ceramic screws (zirconium oxide; Pfannenstiel, Germany). Postoperatively, animals were placed in large, specially designed recovery chairs for 3 days, during which they were taken for walks by the animal caretakers 2 to 3 times per day. The chairs allowed the animals to freely move body and hands, but prevented them from touching the implants. As a prophylactic measure, antibiotics (enrofloxacin; Baytril) and analgesics (flunixin; Finadyne) were administered for 5 days. All surgical procedures were carried out under general balanced anesthesia, whose induction and maintenance was done by trained and qualified personnel. Detailed descriptions of our procedures can be also found in the website of our institute (http://www.hirnforschung.kyb.mpg.de/en/homepage.html). All experimental and surgical...