All animals purposefully navigate feature-rich environments: while exploring, in search of vital resources of food and water, finding mates, and patrolling and marking habitats. During these complex behaviors, continuous analogue input information from peripheral sensory organs guides discrete and digital sequential motor output; accordingly, each action is informed, modulated, or initiated by perceptions of incoming sensory input. In turn, each action can alter the sensory stream itself, by controlling the arrangement of the sensor with the space it is sampling. This entanglement of sensory and motor spaces, creating loops and evolutionary adaptive interactions, is a fundamental function that nervous systems exquisitely display. Uncovering generalizable principles and computational processes of these interactions through neurophysiological, genetic, and behavioral studies, is one of the contemporary challenges of Neuroscience research. However, tools and paradigms to study naturalistic complex behaviors are still lacking, with much of decades long research having been established in reductionist experiments. Even though in restricted laboratory settings, these prior crucial findings have shown remarkable adaptability and rich structures for both animal behavior and neural representations of sensory space. Two major achievements in our quest to understand nervous systems have been the uncovering of sensory and motor maps, represented in hierarchical stages of ascending neural pathways, and the discovery of higher order representations of spatial arrangement of the body in space. Mounting evidence has shown the dependance of these representations on environment context and learning, suggesting different neural computational modes when animals are engaged in more demanding and complex naturalistic behaviors. These types of experiments remain to be performed and are increasingly becoming technologically viable. The genetically tractable and behaviorally amenable rodents have been and continue to be the model of choice for behavioral and sensorimotor research. One of the aims of the work presented here is to introduce behavioral paradigms and tools to investigate complex naturalistic sensorimotor behaviors in rodents. In particular, the rodent trigeminal modality, with its whisker system, has been uniquely useful for studying active sensing. Rodents, like mice and rats, actively sweep their vibrissae arrays and employ them in an array of ethologically important sensorimotor behaviors. These include social behavior, prey capture, purposeful haptic environment interactions, and goal-oriented exploratory behaviors, all complex behaviors that display coordination of body kinematics with the active sensor movements, besides displaying body kinematics continuously guided by whisking input. Thus, working as analogue active sensors, arranged in arrays on each side of the animal’s snout, whiskers provide a rapid and modifiable mechanosensation of the proximal haptic world. Because the topographic arrangement of whiskers on the face is mirrored in somatotopically organized nuclei in neural space, along multiple parallel ascending pathways and along the entire sensory axis from brainstem to cortex, the trigeminal system is also well suited to studying parallelization of sensory streams and functional roles for organization of sensory input into ordered and hierarchical maps. Previous and current work has been largely focused on neural representations of stimulus space in anesthetized or restrained animals, and characterization of behavioral parameters in restrained setups or trained paradigms. In contrast, the work described here focuses on the role of trigeminal sensory information in freely moving animals, and how genetic disruption of topographical sensory organization along selective trigeminal pathways impacts natural and complex sensorimotor behaviors. We show this first in ingestive orosensory behaviors, building on pioneering earlier deafferentation studies. We confirm a crucial role for trigeminal input in eating and drinking. Our results show that trigeminal sensation modulates ingestive motor output at fast timescales. We expand these results and quantify efficiency and precision deficits across ingestive behaviors and across timescales, from milliseconds to months. This work suggests that ordered assembly of trigeminal sensory information, specifically along one of the trigeminal pathways, is critical for the rapid and precise modulation of motor circuits driving eating and drinking action sequences. We next make use of the same genetic mouse model, in addition to wildtype animals, to lay the groundwork for investigating the role of sensory organization in naturalistic and complex volumetric sensorimotor behaviors, focusing on whisking behaviors. This work describes an array of behavioral paradigms, a novel and flexible behavioral setup and methodology for conducting haptic exploratory behaviors where all degrees of movements are available to the animal, in full three-dimensional space. In these experiments, environment context and untrained self-initiated sensorimotor interactions can be studied. We illustrate some results on whisking kinematics and show and discuss advances on tracking whisking and animal behavior. In summary, taken together, we hope that the work presented here will advance our understanding of the functional importance of topographic organization along specific somatosensory pathways. We also expect that the methodology and work described, and the data collected, will provide a rich repository for future studies and enable investigation of crucial sensorimotor questions. We encourage the field to push the envelope and increase the proportion of studies that focus on naturalistic complex, multimodal behaviors. Immediate future results can focus on how head and body parts orientation and movements during our volumetric haptic exploration datasets, are coordinated with the active sensing movements of whiskers. We hope that coupling of active sensory and motor spaces can be investigated, models and hypotheses can be tested, and that exciting new tools and paradigms can build on our work to investigate questions of neural and behavioral computations, including latent learning. The rodent trigeminal system and whisking behaviors have already shown the rich complexities and adaptabilities in both behavior and neural spaces. Cracking open and modelling their complex behavioral processes and sensorimotor loops is one of the next main big and exciting challenges for Neuroscience. Our understanding of neural systems, their function, cognition, and intelligence is dependent on these advancements.

Creator

• Resulaj, Admir

DOI

• https://doi.org/10.21985/n2-2pwr-6739

Subject

• Neurosciences

Language

• en

Alternate Identifier

• etdadmin_upload_879817
• http://dissertations.umi.com/northwestern:15946

Keyword

• Rodent
• Behavior
• Trigeminal
• Prrxl1
• Somatotopy
• Ingestive

Date created

• 2022-01-01

Resource type

• Dissertation

Rights statement

• In Copyright