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Chasing the Cortical Assembly Chasing the Cortical Assembly Damian J. Wallace, PhD, and Jason N. D. Kerr, PhD Network Imaging Group Max Planck Institute for Biological Cybernetics Tübingen, Germany © 2012 Kerr Chasing the Cortical Assembly 43 Introduction NOTES Why is the cortex so difficult to understand? Although involves populations of neurons that are thought to we know enormous amounts of detailed information form a percept of a stimulus. about the neurons that make up the cortex, placing this information back into context of the behaving The most influential theory regarding how activity animal is a serious challenge. In this chapter, we aim in individual neurons may translate into percept to outline some recent technical advances that may formation, the cell assembly hypothesis, was light the way toward the chase for the functional originally conceived by D. O. Hebb in 1949 (Hebb, ensemble. We summarize the progress that has been 1949). Hebb’s functional cell assembly hypothesis made using optical recording approaches with a view aimed to provide a mechanistic and anatomically to what can be expected in the near future, given relevant explanation of how groups of neurons, the recent technological advances. The modeling acting together, may form a percept. Through their and theoretical arguments surrounding neuronal multiple connections, Hebb proposed, neurons ensembles have been described in great detail form cell assemblies that are collectively activated previously (Palm, 1982; Braitenberg, 1978; Gerstein by sensory input and form a brief closed system et al., 1989; Harris, 2005; Mountcastle, 1997, 2003; after stimulation has ceased. Activity from each Wickens and Miller, 1997), so we will not review cell assembly can propagate and activate additional them here. connected cell assemblies in sequence, which he termed a “phase sequence,” and this was proposed to Testing Cortical Hypotheses be the core of neuronal representation of a stimulus- Both anatomically (Douglas and Martin, 2004, 2007) based percept (Hebb, 1949). As individual neurons and electrophysiologically (Spruston, 2008), the can leave and join cell assemblies using activity- properties of individual cells that make up the cortex based synaptic plasticity rules, and therefore can be are very well described, albeit mainly from single-cell members of multiple assemblies, the cell assembly recordings or recordings made from cells in isolation. can be dispersed throughout a cortical population Numerous theories about cortical function date back but linked through potentiated synaptic connections to the early part of the 20th century (von Economo (Gerstein et al., 1989; Gerstner et al., 1993). This and Koskinas, 1925; Hebb, 1949; Lorente de No, is where the challenge of testing the cell-assembly 1949; Mountcastle, 1978). Of these theories, very hypothesis lies: locating the neurons involved in few, if any, have been experimentally tested. Why is forming a cell assembly. Testing this hypothesis this? It is at least in part due to the vast scale of the has been exceedingly difficult owing to the vast problem. More importantly, it is not clear whether numbers of neurons potentially involved, as neither the proposed theories are able to generate hypotheses the number nor locations of ensemble members are that are testable using the available methods, or known. alternatively whether these theories are too general to generate testable hypotheses. Members of functional neuronal ensembles, in any of the proposed theories of cortical function, The basic anatomical pathways and connectivity are dispersed within neuronal populations, and no between cortical areas and cortical layers are systematic anatomical organization within these reasonably well characterized (Braitenberg and ensembles has yet been described. It is thus generally Schüz, 1991; Braitenberg et al., 1998). However, it thought that increasing the numbers of neurons is the firing of action potentials (APs) that defines from which simultaneous recordings are made will the functional cortical characteristics, moment by increase the chances of capturing many members of moment, through these pathways. APs propagate an ensemble (Grewe and Helmchen, 2009). Given throughout an individual neuron’s entire axonal that it is not clear how many members make up a arbor (Cox et al., 2000; Koester and Sakmann, 2000), neuronal ensemble or whether the same neurons are and probably influence all postsynaptic partners. involved from one trial to another, we suggest that Individual postsynaptic neurons receive and integrate this is only part of the picture. Making measurements a vast number of inputs from presynaptic neurons at from functional neuronal ensembles during cortical any moment (Hasenstaub et al., 2005; Waters and computation is likely to require multiple techniques Helmchen, 2006). Although individual neurons capable of recording from, locating, and potentially have considerable computational capacity (Larkum manipulating the activity of individual neurons and Nevian, 2008; Losonczy et al., 2008; Jia et al., embedded within large populations. Although a 2010), neuronal processing of sensory information multitude of new technical advances can be applied © 2012 Kerr 44 NOTES to locating the neuronal assembly (improved • The ability to record from the same neurons over transynaptic tracing being an example), the question many days (Mank et al., 2008; Tian et al., 2009; arises: Are we any closer to recording from, or Andermann et al., 2010). understanding, the Hebbian cell assembly and its role in sensory coding? More recently, several groups have extended multiphoton population imaging to the study Lighting the Cortical Ensemble of several animal models: the awake head-fixed Multiphoton imaging (Greenberg et al., 2008), head-fixed and behaving (Andermann et al., 2010; Komiyama et al., 2010), One of the biggest recent advances in the ability to head-fixed but mobile (Dombeck et al., 2007, 2009), record activity simultaneously from many neurons and freely moving animal (Sawinski et al., 2009). If in vivo (Stosiek et al., 2003), with single-cell and detection of AP firing is central to detecting neurons single-AP accuracy (Kerr et al., 2005), has come from involved in a cell assembly, in which individual multiphoton imaging (Denk et al., 1990; Svoboda members could change with each trial, then imaging et al., 1997; Kerr and Denk, 2008). Its three main must be able to accurately resolve activity on a trial- advantages are as follows: by-trial basis to enable capture of activity related to neuronal assembly. • The ability to infer electrical activity from all neurons within a local area on a trial-by-trial basis (Kerr et al., 2007; Sato et al., 2007; Rothschild et Inferring action potential al., 2010); All activity-based population recordings have used either bolus loading of synthetic fluorescent Ca2+- • Known spatial location of all the recorded neurons indicator dyes (Stosiek et al., 2003) (Fig. 1a–b) or 2+ (Ohki et al., 2005; Mrsic-Flogel et al., 2007); infection of cells with genetically encoded Ca indicators (Hasan et al., 2004; Mank et al., 2008; • The capacity to record activity from neurons that Wallace et al., 2008; Tian et al,. 2009). These fire at low rates (Kerr et al., 2005; Greenberg et al., indicators typically label populations of hundreds of 2008); and neurons in areas covering ~500 × 500 × 500 μm (Kerr and Denk, 2008). Although the indicators report Figure 1. (see opposite page) Imaging neuronal activity. a, Two-photon image of a population of cortical cells labeled with the fluorescent Ca2+ indicator Oregon green BAPTA-1. Astrocytes are counterstained with Sulforhodamine 101 (yellow/red), while neurons appear green. b, Ca2+ transients simultaneously recorded from a population of 13 neurons in vivo. c, Simultaneous Ca2+ imaging and cell-attached electrophysiological recording in vivo showing Ca2+ transients associated with single APs and doublets. Simultaneous electrophysiological recording is essential to accurately calibrate algorithms designed to convert the Ca2+ traces observed in in vivo recordings from populations of neurons into accurate AP raster plots. The simultaneously recorded Ca2+ trace and extracellular electrophysiology are shown to the right, with the model output from the spike-detection algo- rithm (described in Greenberg et al., 2008) corresponding to the Ca2+ trace (green). d–e, Infrared images and Ca2+ transients recorded in neurons in the forelimb representation of the primary motor cortex in a head-fixed mouse on a spherical treadmill. d, Infrared video images showing forepaw movements during typical grooming and running behavior. e, Baseline subtracted Ca2+ traces (black) with significant transients detected using the detection method employed (orange). In Dombeck et al. (2009), two independent analysis methods were used to provide compelling evidence for functional clustering of neurons preferentially active during running or grooming behaviors. f–h, High-speed in vivo two-photon imaging of neuronal activity using an AOD scanning system. f, Overview image of a field of labeled neurons, highlighting a group of 7 cells on an irregular scan path from which data were collected. g, Ca2+-imaging traces from the correspondingly numbered neurons in panel f. h, Graph showing the relationship between cellwise sampling rate and number of cells scanned when the number of acquisition points in each cell is varied from 3 to 9. Using this AOD scanning approach, ~100 cells can be scanned in vivo with a cellwise acquisition
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