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Visualizing Adult Cortical Plasticity Using Intrinsic Signal Optical Imaging

In: In Vivo Optical Imaging of Brain Function. 2nd edition. Boca Raton (FL): CRC Press/Taylor & Francis; 2009. Chapter 9.

Visualizing Adult Cortical Plasticity Using Intrinsic Signal Optical Imaging

Ron D. Frostig et al.


Our understanding of the functional organization and plasticity of the adult sensory cortex has been transformed in the last 25 years. The view that cortical functional representations of the sensory surface in adult animals are fixed, especially for the primary sensory cortices, has been replaced by the view that they are dynamic and continuously modified by the animal’s experience. Such “experience-dependent” plasticity in adult cortical functional representations has been demonstrated in a range of mammalian species across many primary cortices and has been implicated in a range of fundamental processes including rehabilitation following peripheral sensory loss or damage, recoveries from central nervous system damage, improvements in sensory-motor skills with practice, and learning and memory, thus underscoring its importance to an organism’s survival. For recent reviews on adult cortical plasticity see References [1,2]. While much progress has been made in understanding the phenomenology and underlying mechanisms, research on the plasticity of adult cortical functional representations is still in its infancy. So far, several techniques have been available for the study of adult cortical plasticity. Ideally, a technique should have the ability to sample: (1) neuronal spiking activity, (2) noninvasively, (3) simultaneously from large cortical regions, (4) with high, 3D spatial resolution, (5) and high temporal resolution, (6) in the awake animal. This ideal technique would enable the direct, noninvasive (hence, long-term and nondamaging) assessment of a cortical functional representation (comprised of many neurons collectively occupying a volume of cortex) with sufficient spatial and temporal resolution to track real-time changes in the functional representation in the awake, behaving animal. In recent years, there has been a growing interest also in studying evoked subthreshold activity, and therefore the ability to record subthreshold activation should be added to the above list of abilities of the ideal technique for studying cortical plasticity. Unfortunately, such an ideal technique does not exist but each of the most widely used current techniques for studying cortical plasticity offers a particular subset of the just-described advantages. The most popular technique is the use of a single microelectrode to record from the cortex. It offers the advantage of recording action potentials and subthreshold activity directly from cortical neurons with high spatial (point) and temporal (ms) resolution sufficient to follow real-time changes in neuronal activity at any location along a volume of cortex, with the disadvantage that recordings are invasive to the cortex. In order to assess the functional representation of a sensory organ (e.g., a finger, a whisker), neurons are recorded from different cortical locations and the functional representation of the organ is then defined as the cortical region containing neurons responsive to stimulation of that organ (i.e., neurons that have receptive fields localized at the sensory organ). A change in the spatial distribution of neurons responsive to a given sensory organ and/or in their amplitude of response is typically taken as evidence for plasticity in the functional representation of that sensory organ [3]. As a cortical functional representation could be comprised of thousands to millions of neurons distributed over a volume of cortex, the use of a single micro-electrode to characterize the plasticity of a functional representation requires many recordings across a large cortical region, recordings that can only be obtained in a serial fashion and require many hours to complete; thus, the animal is typically anesthetized. Because the number of recordings will be limited due to cortical tissue damage incurred during the experiment and time constraints, the characterization of a functional representation is dependent on the extrapolation between recording locations. Also, because of its invasiveness, this technique is not ideal for the assessment of the same functional representation before and after a manipulation within the same animal. The recent development of simultaneous recordings from a chronically implanted array of microelectrodes (see review [4]) provides relief to some of the challenges described above, and has great promise for its potential for long-term recordings from the same animal, although recordings still damage the cortical tissue, the sample size is still small, and extrapolation is still needed between recording locations. Therefore, for better understanding of large-scale cortical functional organization and its plasticity, microelectrode arrays are still limited in fulfilling the need for visualizing mass-action of millions of neurons at different points in time before, during, and after an experimental manipulation. In this chapter we discuss in detail how visualizing the activity from a large population of neurons can be achieved with our principal technique for studying plasticity of adult cortical functional representations known as intrinsic signal optical imaging (ISOI) [5,6,7], with examples of its applications for functional imaging of rat primary somatosensory cortex. ISOI lacks the ability to directly measure neuronal activity (spiking or subthreshold) and track data in millisecond temporal resolution, but is capable of visualizing functional representations via the simultaneous sampling of a large cortical region with high spatial resolution. We find the combined use of ISOI with rat primary somatosensory cortex particularly appealing because: (1) this animal model offers many advantages for the study of adult cortical plasticity, (2) it can be noninvasive to the cortical tissue (by imaging through the skull) and thus offers the opportunity to image chronically from the same animal, and (3) it is capable of visualizing functional representations in real time (albeit providing only an aerial, i.e. two-dimensional, view of functional representations) and exploits a signal source that appears to be more closely related to underlying spiking activity. The remainder of the chapter is devoted to describing the background, theory and methodological issues relevant to imaging cortical functional representations, the successful application of ISOI for studying the plasticity of whiskers functional representations in the adult rat, and potential future directions for ISOI.

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