Responses to auditory stimuli in macaque lateral intraparietal area

The lateral intraparietal area (LIP) of macaque posterior parietal cortex participates in the sensorimotor transformations underlying visually guided eye movements. Area LIP has long been considered unresponsive to auditory stimulation. However, recent studies have shown that neurons in LIP respond to auditory stimuli during an auditory-saccade task, suggesting possible involvement of this area in auditory-to-oculomotor as well as visual-to-oculomotor processing. This dissertation describes investigations which clarify the role of area LIP in auditory-to-oculomotor processing.

Extracellular recordings were obtained from a total of 332 LIP neurons in two macaque monkeys, while the animals performed fixation and saccade tasks involving auditory and visual stimuli. No auditory activity was observed in area LIP before animals were trained to make saccades to auditory stimuli, but responses to auditory stimuli did emerge after auditory-saccade training. Auditory responses in area LIP after auditory-saccade training were significantly stronger in the context of an auditory-saccade task than in the context of a fixation task. Compared to visual responses, auditory responses were also significantly more predictive of movement-related activity in the saccade task. Moreover, while visual responses often had a fast transient component, responses to auditory stimuli in area LIP tended to be gradual in onset and relatively prolonged in duration.

Overall, the analyses demonstrate that responses to auditory stimuli in area LIP are dependent on auditory-saccade training, modulated by behavioral context, and characterized by slow-onset, sustained response profiles. These findings suggest that responses to auditory stimuli are best interpreted as supramodal (cognitive or motor) responses, rather than as modality-specific sensory responses. Auditory responses in area LIP seem to reflect the significance of auditory stimuli as potential targets for eye movements, and may differ from most visual responses in the extent to which they arc abstracted from the sensory parameters of the stimulus.

Neural representation of auditory temporal structure

Neurons in the songbird forebrain nucleus HVc are highly sensitive to auditory temporal context and have some of the most complex auditory tuning properties yet discovered. HVc is crucial for learning, perceiving, and producing song, thus it is important to understand the neural circuitry and mechanisms that give rise to these remarkable auditory response properties. This thesis investigates these issues experimentally and computationally.

Extracellular studies reported here compare the auditory context sensitivity of neurons in HV c with neurons in the afferent areas of field L. These demonstrate that there is a substantial increase in the auditory temporal context sensitivity from the areas of field L to HVc. Whole-cell recordings of HVc neurons from acute brain slices are described which show that excitatory synaptic transmission between HVc neurons involve the release of glutamate and the activation of both AMPA/kainate and NMDA-type glutamate receptors. Additionally, widespread inhibitory interactions exist between HVc neurons that are mediated by postsynaptic GABA_A receptors. Intracellular recordings of HVc auditory neurons in vivo provides evidence that HV c neurons encode information about temporal structure using a variety of cellular and synaptic mechanisms including syllable-specific inhibition, excitatory post-synaptic potentials with a range of different time courses, and burst-firing, and song-specific hyperpolarization.

The final part of this thesis presents two computational approaches for representing and learning temporal structure. The first method utilizes comput ational elements that are analogous to temporal combination sensitive neurons in HVc. A network of these elements can learn using local information and lateral inhibition. The second method presents a more general framework which allows a network to discover mixtures of temporal features in a continuous stream of input.

Contributions of parietal cortex to reach planning

Sensory-motor circuits course through the parietal cortex of the human and monkey brain. How parietal cortex manipulates these signals has been an important question in behavioral neuroscience. This thesis presents experiments that explore the contributions of monkey parietal cortex to sensory-motor processing, with an emphasis on the area's contributions to reaching. First, it is shown that parietal cortex is organized into subregions devoted to specific movements. Area LIP encodes plans to make saccadic eye movements. A nearby area, the parietal reach region (PRR), plans reaches. A series of experiments are then described which explore the contributions of PRR to reach planning. Reach plans are represented in an eye-centered reference frame in PRR. This representation is shown to be stable across eye movements. When a sequence of reaches is planned, only the impending movement is represented in PRR, showing that the area is more related to movement planning than to storing the memory of reach targets. PRR resembles area LIP in each of these properties: the two areas may provide a substrate for hand-eye coordination. These findings yield new perspectives on the functions of the parietal cortex and on the organization of sensory-motor processing in primate brains.

Neural Prosthetics and Parietal Cortex

In the last decade, research efforts into directly interfacing with the neurons of individuals with motor deficits have increased. The goal of such research is clear: Enable individuals affected by paralysis or amputation to regain control of their environments by manipulating external devices with thought alone. Though the motor cortices are the usual brain areas upon which neural prosthetics depend, research into the parietal lobe and its subregions, primarily in non-human primates, has uncovered alternative areas that could also benefit neural interfaces. Similar to the motor cortical areas, parietal regions can supply information about the trajectories of movements. In addition, the parietal lobe also contains cognitive signals like movement goals and intentions. But, these areas are also known to be tuned to saccadic eye movements, which could interfere with the function of a prosthetic designed to capture motor intentions only. In this thesis, we develop and examine the functionality of a neural prosthetic with a non-human primate model using the superior parietal lobe to examine the effectiveness of such an interface and the effects of unconstrained eye movements in a task that more closely simulates clinical applications. Additionally, we examine methods for improving usability of such interfaces.

The parietal cortex is also believed to contain neural signals relating to monitoring of the state of the limbs through visual and somatosensory feedback. In one of the world’s first clinical neural prosthetics based on the human parietal lobe, we examine the extent to which feedback regarding the state of a movement effector alters parietal neural signals and what the implications are for motor neural prosthetics and how this informs our understanding of this area of the human brain.