The fronto-parietal grasping network

One potential way to select a cortical network to record from is based on the behavior which is generated and controlled by it. Ideally the behavior is measurable and quantifiable, such as overt motor movements. Grasp movements are one of the most important for interacting with our environment on an everyday basis. The cortical network which generates and controls grasp movements includes as some of its core areas of the anterior intraparietal area (AIP), the ventral premotor cortex (F5), and the primary motor cortex (M1). AIP and F5 are part of the fronto-parietal network and are known to be strongly reciprocally connected, as are F5 and M1 (Luppino et al., 1999). Inactivation studies of area AIP and F5 showed deficits in pre-shaping of the hand during grasping, confirming them to be involved in grasp generation and control (Gallese et al., 1994; Fogassi et al., 2001). Several studies have been conducted on monkeys trained to do visual fixation tasks as well as visually guided delayed or non-delayed grasping tasks while single neuron activity was recorded in AIP and F5. These studies showed that neurons of both areas were modulated for visual object discrimination (Murata et al., 2000; Janssen and Scherberger, 2015), movement preparation (Baumann et al., 2009; Fluet et al., 2010), and movement related processing (Menz et al., 2015). These findings are well in line with the information representation of neurons recorded from the fronto-parietal networks for saccadic eye movements (LIP and FEF) (Freedman and Assad, 2006; Siegel et al., 2015) and for reach moments (PRR and PMd) (Gail, 2006; Churchland et al., 2010; 2012). The presence of visual and preparatory activity within the same network led to the assumption that AIP and F5 play an important role in visuo-motor transformation (Janssen and Scherberger, 2015), also well in line with findings from studies of the fronto-parietal saccadic eye movement and reaching network. Strong evidence for this idea was provided by two studies showing that, in the fronto-parietal grasping network including M1, visual information was found to be most strongly represented in AIP, followed by F5, and movement related information was most strongly represented in M1, followed by F5, and most weakly in AIP (Schaffelhofer et al., 2015; Schaffelhofer and Scherberger, 2016). These findings suggest a graded representation and transformation of neuronal information across the areas, again in agreement with studies of the fronto-parietal saccadic eye movement network (Siegel et al., 2015). Interestingly, information relevant to reach and eye position was found to be encoded by the population of neurons in F5 and AIP (Lehmann and Scherberger, 2013), further suggesting a graded representation for the controlled motor

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moment across the whole fronto-parietal network. A potential reason for this overlapping representation, which was also found for eye and reach representation and coordination in LIP and PRR (Andersen and Cui, 2009), could be that flexible coordination of eye, reach, and grasp movements is necessary in everyday life. The high degree of similarity between the fronto-parietal saccadic eye movement, reaching, and grasping networks, as well as the overlap between them, suggests AIP and F5 are also involved in decision making.

Taken together, neurons in the fronto-parietal grasping network are selective for visual, preparatory, and grasp movement related information and are involved in the transformation from visual to preparatory activity, from preparatory to movement activity, and very likely also in the decision making process that are part of these transformations.

Conveniently, the involvement of this network in grasp movement preparation and generation allows for the direct measurement and quantification of the output of the system. Furthermore, there is evidence for beta-band synchronization originating from parietal regions such as AIP, which potentially is an important coordinative mechanism involved in decision making and movement intentions, as mentioned before. However, the exact interplay of all these processes is currently not well understood (Janssen and

Scherberger, 2015), positioning the fronto-parietal grasping network of macaque monkeys as a suitable structure to study the encoding, transformation, and coordination of

information and decision making. Such studies will provide the characterizations needed to better understand the formation of functional neuronal ensembles.

In order to explore these processes leading to clearer comprehension of functional neuronal ensembles within the fronto-parietal grasping network large populations of neurons of this network were recorded in parallel as a databasis of this thesis, while monkeys performed different delayed grasping tasks. Four monkeys were trained on two different tasks and were chronically implanted with four to six floating microelectrode arrays with 36 electrodes (Figure 3) in AIP, F5 and in one case M1 (two per area). The signal of all electrodes were recorded in parallel and as a basis of all performed analyses large

populations of neurons were extracted via spike-sorting algorithm (Figure 5).

In chapter 2.1 the coordination of the information flow across the fronto-parietal single neuron network was analyzed by estimating the the directed functional connectivity between all pairs of single neurons. The kind of synchronization process was analyzed together with the functional network topology allowing for a unifying view of both aspects.

In chapter 2.2 the encoding of information across the neuronal population of AIP and F5 was analyzed, while two monkeys performed a mixed instructed and free-choice delayed grasping task. Analyses of the classical representational framework were contrasted with population analyses in line with the dynamical system perspective. Furthermore, a

regularized RNN model was trained for the same conditions to produce muscle activity for the performed grip types. This model offered a biological plausible explanation for decision related transformation of information within the fronto-pariatal grasping network.

In chapter 2.3 the neuronal population dynamics across AIP and F5 of two monkeys were analyzed of the transition between immediate and delayed grasp movements.

Population analyses by using dimensionality reduction techniques revealed how dynamical as well as static aspects of movement preparation can be encoded simultaneously in different dimensions in the same neuronal state space.

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