Biological Pattern Generation: The Cellular and Computational Logic of Networks in Motion

In 1900, Ramón y Cajal advanced the neuron doctrine, defining the neuron as the fundamental signaling unit of the nervous system. Over a century later, neurobiologists address the circuit doctrine: the logic of the core units of neuronal circuitry that control animal behavior. These are circuits that can be called into action for perceptual, conceptual, and motor tasks, and we now need to understand whether there are coherent and overriding principles that govern the design and function of these modules. The discovery of central motor programs has provided crucial insight into the logic of one prototypic set of neural circuits: those that generate motor patterns. In this review, I discuss the mode of operation of these pattern generator networks and consider the neural mechanisms through which they are selected and activated. In addition, I will outline the utility of computational models in analysis of the dynamic actions of these motor networks

A cambrian origin for vertebrate rods

Vertebrates acquired dim light vision when an ancestral cone evolved into the rod photoreceptor at an unknown stage preceding the last common ancestor of extant jawed vertebrates (~420 million years ago Ma). The jawless lampreys provide a unique opportunity to constrain the timing of this advance, as their line diverged ~505 Ma and later displayed high morphological stability. We recorded with patch electrodes the inner segment photovoltages and with suction electrodes the outer segment photocurrents of Lampetra fluviatilis retinal photoreceptors. Several key functional features of jawed vertebrate rods are present in their phylogenetically homologous photoreceptors in lamprey: crucially, the efficient amplification of the effect of single photons, measured by multiple parameters, and the flow of rod signals into cones. These results make convergent evolution in the jawless and jawed vertebrate lines unlikely and indicate an early origin of rods, implying strong selective pressure toward dim light vision in Cambrian ecosystems

Conserved subcortical processing in visuo-vestibular gaze control

Gaze stabilization compensates for movements of the head or external environment to minimize image blurring. Multisensory information stabilizes the scene on the retina via the vestibulo-ocular (VOR) and optokinetic (OKR) reflexes. While the organization of neuronal circuits underlying VOR is well-described across vertebrates, less is known about the contribution and evolution of the OKR and the basic structures allowing visuo-vestibular integration. To analyze these neuronal pathways underlying visuo-vestibular integration, we developed a setup using a lamprey eye-brain-labyrinth preparation, which allowed coordinating electrophysiological recordings, vestibular stimulation with a moving platform, and visual stimulation via screens. Lampreys exhibit robust visuo-vestibular integration, with optokinetic information processed in the pretectum that can be downregulated from tectum. Visual and vestibular inputs are integrated at several subcortical levels. Additionally, saccades are present in the form of nystagmus. Thus, all basic components of the visuo-vestibular control of gaze were present already at the dawn of vertebrate evolution.Swedish Medical Research Council | Ref. VR-M-K2013-62X-03026Swedish Medical Research Council | Ref. VR-M-2015-02816Swedish Medical Research Council | Ref. VR-M-2018-02453Swedish Medical Research Council | Ref. VR-M-2019-01854Ministerio de Ciencia e Innovación | Ref. PID2020-113646GA-I00Ministerio de Ciencia e Innovación | Ref. RYC2018-024053 -IXunta de Galicia | Ref. ED431B 2021/04European Commission | Ref. EU/FP7, n. 316639European Commission | Ref. Horizon 2020, n. 720270European Commission | Ref. Horizon 2020, n. 785907European Commission | Ref. Horizon 2020, n. 945539Gösta Fraenckel Foundation for Medical Research | Ref. FS-2020:000

The tectum/superior colliculus as the vertebrate solution for spatial sensory integration and action

The superior colliculus, or tectum in the case of non-mammalian vertebrates, is a part of the brain that registers events in the surrounding space, often through vision and hearing, but also through electrosensation, infrared detection, and other sensory modalities in diverse vertebrate lineages. This information is used to form maps of the surrounding space and the positions of different salient stimuli in relation to the individual. The sensory maps are arranged in layers with visual input in the uppermost layer, other senses in deeper positions, and a spatially aligned motor map in the deepest layer. Here, we will review the organization and intrinsic function of the tectum/superior colliculus and the information that is processed within tectal circuits. We will also discuss tectal/superior colliculus outputs that are conveyed directly to downstream motor circuits or via the thalamus to cortical areas to control various aspects of behavior. The tectum/superior colliculus is evolutionarily conserved among all vertebrates, but tailored to the sensory specialties of each lineage, and its roles have shifted with the emergence of the cerebral cortex in mammals. We will illustrate both the conserved and divergent properties of the tectum/superior colliculus through vertebrate evolution by comparing tectal processing in lampreys belonging to the oldest group of extant vertebrates, larval zebrafish, rodents, and other vertebrates including primates

Reinforcement Learning in a Spiking Neural Model of Striatum Plasticity

The basal ganglia (BG), and more specifically the striatum, have long been proposed to play an essential role in action-selection based on a reinforcement learning (RL) paradigm. However, some recent findings, such as striatal spike-timing-dependent plasticity (STDP) or striatal lateral connectivity, require further research and modelling as their respective roles are still not well understood. Theoretical models of spiking neurons with homeostatic mechanisms, lateral connectivity, and reward-modulated STDP have demonstrated a remarkable capability to learn sensorial patterns that statistically correlate with a rewarding signal. In this article, we implement a functional and biologically inspired network model of the striatum, where learning is based on a previously proposed learning rule called spike-timing-dependent eligibility (STDE), which captures important experimental features in the striatum. The proposed computational model can recognize complex input patterns and consistently choose rewarded actions to respond to such sensorial inputs. Moreover, we assess the role different neuronal and network features, such as homeostatic mechanisms and lateral inhibitory connections, play in action-selection with the proposed model. The homeostatic mechanisms make learning more robust (in terms of suitable parameters) and facilitate recovery after rewarding policy swapping, while lateral inhibitory connections are important when multiple input patterns are associated with the same rewarded action. Finally, according to our simulations, the optimal delay between the action and the dopaminergic feedback is obtained around 300 ms, as demonstrated in previous studies of RL and in biological studies

The Lamprey Pallium Provides a Blueprint of the Mammalian Motor Projections from Cortex

SummaryBackgroundThe frontal lobe control of movement in mammals has been thought to be a specific function primarily related to the layered neocortex with its efferent connections. In contrast, we now show that the same basic organization is present even in one of the phylogenetically oldest vertebrates, the lamprey.ResultsStimulation of specific sites in the pallium/cortex evokes eye, trunk, locomotor, or oral movements. The pallial projection neurons target brainstem motor centers and basal ganglia subnuclei and have prominent dendrites extending into the outer molecular layer. They exhibit the characteristic features of pyramidal neurons and elicit monosynaptic glutamatergic excitatory postsynaptic potentials in output neurons of the optic tectum, reticulospinal neurons, and, as shown earlier, basal ganglia neurons.ConclusionsOur results demonstrate marked similarities in the efferent functional connectivity and control of motor behavior between the lamprey pallium and mammalian neocortex. Thus, the lamprey motor pallium/cortex represents an evolutionary blueprint of the corresponding mammalian system