scholarly journals Complexity of frequency receptive fields predicts tonotopic variability across species

eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Quentin Gaucher ◽  
Mariangela Panniello ◽  
Aleksandar Z Ivanov ◽  
Johannes C Dahmen ◽  
Andrew J King ◽  
...  

Primary cortical areas contain maps of sensory features, including sound frequency in primary auditory cortex (A1). Two-photon calcium imaging in mice has confirmed the presence of these global tonotopic maps, while uncovering an unexpected local variability in the stimulus preferences of individual neurons in A1 and other primary regions. Here we show that local heterogeneity of frequency preferences is not unique to rodents. Using two-photon calcium imaging in layers 2/3, we found that local variance in frequency preferences is equivalent in ferrets and mice. Neurons with multipeaked frequency tuning are less spatially organized than those tuned to a single frequency in both species. Furthermore, we show that microelectrode recordings may describe a smoother tonotopic arrangement due to a sampling bias towards neurons with simple frequency tuning. These results help explain previous inconsistencies in cortical topography across species and recording techniques.

2019 ◽  
Author(s):  
Quentin Gaucher ◽  
Mariangela Panniello ◽  
Aleksandar Z Ivanov ◽  
Johannes C Dahmen ◽  
Andrew J King ◽  
...  

AbstractPrimary cortical areas contain maps of sensory features, including sound frequency in primary auditory cortex (A1). Two-photon calcium imaging in mice has confirmed the presence of these large-scale maps, while uncovering an unexpected local variability in the stimulus preferences of individual neurons in A1 and other primary regions. Here we show that fractured tonotopy is not unique to rodents. Using two-photon imaging, we found that local variance in frequency preferences is equivalent in ferrets and mice. Much of this heterogeneity was due to neurons with complex frequency tuning, which are less spatially organized than those tuned to a single frequency. Finally, we show that microelectrode recordings may describe a smoother tonotopic arrangement due to a bias towards neurons with simple frequency tuning. These results show that local variability in the tonotopic map is not restricted to rodents and help explain inconsistencies in cortical topography across species and recording techniques.


2016 ◽  
Vol 116 (2) ◽  
pp. 431-437 ◽  
Author(s):  
Charles G. Frye ◽  
Jason N. MacLean

Spontaneous propagation of spiking within the local neocortical circuits of mature primary sensory areas is highly nonrandom, engaging specific sets of interconnected and functionally related neurons. These spontaneous activations promise insight into neocortical structure and function, but their properties in the first 2 wk of perinatal development are incompletely characterized. Previously, we have found that there is a minimal numerical sample, on the order of 400 cells, necessary to fully capture mature neocortical circuit dynamics. Therefore we maximized our numerical sample by using two-photon calcium imaging to observe spontaneous activity in populations of up to 1,062 neurons spanning multiple columns and layers in 52 acute coronal slices of mouse neocortex at each day from postnatal day (PND) 3 to PND 15. Slices contained either primary auditory cortex (A1) or somatosensory barrel field (S1BF), which allowed us to compare sensory modalities with markedly different developmental timelines. Between PND 3 and PND 8, populations in both areas exhibited activations of anatomically compact subgroups on the order of dozens of cells. Between PND 9 and PND 13, the spatiotemporal structure of the activity diversified to include spatially distributed activations encompassing hundreds of cells. Sparse activations covering the entire field of view dominated in slices taken on or after PND 14. These and other findings demonstrate that the developmental progression of spontaneous activations from active local modules in the first postnatal week to sparse, intermingled groups of neurons at the beginning of the third postnatal week generalizes across primary sensory areas, consistent with an intrinsic developmental trajectory independent of sensory input.


2012 ◽  
Vol 107 (3) ◽  
pp. 923-936 ◽  
Author(s):  
Ian Nauhaus ◽  
Kristina J. Nielsen ◽  
Edward M. Callaway

We studied the relative accuracy of drifting gratings and noise stimuli for functionally characterizing neural populations using two-photon calcium imaging. Calcium imaging has the potential to distort measurements due to nonlinearity in the conversion from spikes to observed fluorescence. We demonstrate a dramatic impact of fluorescence saturation on functional measurements in ferret V1 by showing that responses to drifting gratings strongly violate contrast invariance of orientation tuning, a fundamental property of the spike rates. The observed relationship is consistent with saturation that clips the high-contrast tuning curve peaks by ∼40%. The nonlinearity was also apparent in mouse V1 responses to drifting gratings, but not as strong as in the ferret. Contrast invariance holds, however, for tuning curves measured with a randomized grating stimulus. This finding is consistent with prior work showing that the linear portion of a linear-nonlinear system can be recovered with reverse correlation. Furthermore, we demonstrate that a noise stimulus is more effective at keeping spike rates in the linear operating regime of a saturating nonlinearity, which both maximizes signal-to-noise ratios and simplifies the recovery of fast spike dynamics from slow calcium transients. Finally, we uncover spatiotemporal receptive fields by removing the nonlinearity and slow calcium transient from a model of fluorescence generation, which allowed us to observe dynamic sharpening of orientation tuning. We conclude that for two-photon recordings it is imperative that one considers the nonlinear distortion when designing stimuli and interpreting results, especially in sensory areas, species, or cell types with high firing rates.


eLife ◽  
2020 ◽  
Vol 9 ◽  
Author(s):  
Xiao-lin Chou ◽  
Qi Fang ◽  
Linqing Yan ◽  
Wen Zhong ◽  
Bo Peng ◽  
...  

Lateral posterior nucleus (LP) of thalamus, the rodent homologue of primate pulvinar, projects extensively to sensory cortices. However, its functional role in sensory cortical processing remains largely unclear. Here, bidirectional activity modulations of LP or its projection to the primary auditory cortex (A1) in awake mice reveal that LP improves auditory processing in A1 supragranular-layer neurons by sharpening their receptive fields and frequency tuning, as well as increasing the signal-to-noise ratio (SNR). This is achieved through a subtractive-suppression mechanism, mediated largely by LP-to-A1 axons preferentially innervating specific inhibitory neurons in layer 1 and superficial layers. LP is strongly activated by specific sensory signals relayed from the superior colliculus (SC), contributing to the maintenance and enhancement of A1 processing in the presence of auditory background noise and threatening visual looming stimuli respectively. Thus, a multisensory bottom-up SC-pulvinar-A1 pathway plays a role in contextual and cross-modality modulation of auditory cortical processing.


2009 ◽  
Vol 65 ◽  
pp. S172
Author(s):  
Yoshiya Mori ◽  
Koji Ikezoe ◽  
Junichi Furutaka ◽  
Kazuo Kitamura ◽  
Hiroshi Tamura ◽  
...  

2006 ◽  
Vol 96 (6) ◽  
pp. 2972-2983 ◽  
Author(s):  
Gabriel Soto ◽  
Nancy Kopell ◽  
Kamal Sen

Two fundamental issues in auditory cortical processing are the relative importance of thalamocortical versus intracortical circuits in shaping response properties in primary auditory cortex (ACx), and how the effects of neuromodulators on these circuits affect dynamic changes in network and receptive field properties that enhance signal processing and adaptive behavior. To investigate these issues, we developed a computational model of layers III and IV (LIII/IV) of AI, constrained by anatomical and physiological data. We focus on how the local and global cortical architecture shape receptive fields (RFs) of cortical cells and on how different well-established cholinergic effects on the cortical network reshape frequency-tuning properties of cells in ACx. We identify key thalamocortical and intracortical circuits that strongly affect tuning curves of model cortical neurons and are also sensitive to cholinergic modulation. We then study how differential cholinergic modulation of network parameters change the tuning properties of our model cells and propose two different mechanisms: one intracortical (involving muscarinic receptors) and one thalamocortical (involving nicotinic receptors), which may be involved in rapid plasticity in ACx, as recently reported in a study by Fritz and coworkers.


2001 ◽  
Vol 86 (1) ◽  
pp. 475-491 ◽  
Author(s):  
William C. Loftus ◽  
Mitchell L. Sutter

The excitatory and inhibitory frequency/intensity response areas (FRAs) and spectrotemporal receptive fields (STRFs) of posterior auditory cortical field (PAF) single neurons were investigated in barbiturate anesthetized cats. PAF neurons' pure-tone excitatory FRAs (eFRAs) exhibited a diversity of shapes, including some with very broad frequency tuning and some with multiple distinct excitatory frequency ranges (i.e., multipeaked eFRAs). Excitatory FRAs were analyzed after selectively excluding spikes on the basis of spike response times relative to stimulus onset. This analysis indicated that spikes with shorter response times were confined to narrow regions of the eFRAs, while spikes with longer response times were more broadly distributed over the eFRA. First-spike latencies in higher threshold response peaks of multipeaked eFRAs were ∼10 ms longer, on average, than latencies in lower threshold response peaks. STRFs were constructed to examine the dynamic frequency tuning of neurons. More than half of the neurons (51%) had STRFs with “sloped” response maxima, indicating that the excitatory frequency range shifted with time. A population analysis demonstrated that the median first-spike latency varied systematically as a function of frequency with a median slope of ∼12 ms per octave. Inhibitory frequency response areas were determined by simultaneous two-tone stimulation. As in primary auditory cortex (A1), a diversity of inhibitory band structures was observed. The largest class of neurons (25%) had an inhibitory band flanking each eFRA edge, i.e., one lower and one upper inhibitory band in a “center-surround” organization. However, in comparison to a previous report of inhibitory structure in A1 neurons, PAF exhibited a higher incidence of neurons with more complex inhibitory band structure (for example, >2 inhibitory bands). As was the case with eFRAs, spikes with longer response times contributed to the complexity of inhibitory FRAs. These data indicate that PAF neurons integrate temporally varying excitatory and inhibitory inputs from a broad spectral extent and, compared with A1, may be suited to analyzing acoustic signals of greater spectrotemporal complexity than was previously thought.


Author(s):  
Joshua H. Siegle ◽  
Peter Ledochowitsch ◽  
Xiaoxuan Jia ◽  
Daniel Millman ◽  
Gabriel K. Ocker ◽  
...  

AbstractExtracellular electrophysiology and two-photon calcium imaging are widely used methods for measuring physiological activity with single-cell resolution across large populations of neurons in the brain. While these two modalities have distinct advantages and disadvantages, neither provides complete, unbiased information about the underlying neural population. Here, we compare evoked responses in visual cortex recorded in awake mice under highly standardized conditions using either imaging or electrophysiology. Across all stimulus conditions tested, we observe a larger fraction of responsive neurons in electrophysiology and higher stimulus selectivity in calcium imaging. This work explores which data transformations are most useful for explaining these modality-specific discrepancies. We show that the higher selectivity in imaging can be partially reconciled by applying a spikes-to-calcium forward model to the electrophysiology data. However, the forward model could not reconcile differences in responsiveness without sub-selecting neurons based on event rate or level of signal contamination. This suggests that differences in responsiveness more likely reflect neuronal sampling bias or cluster-merging artifacts during spike sorting of electrophysiological recordings, rather than flaws in event detection from fluorescence time series. This work establishes the dominant impacts of the two modalities’ respective biases on a set of functional metrics that are fundamental for characterizing sensory-evoked responses.


Author(s):  
Misha B. Ahrens ◽  
Kuo Hua Huang ◽  
Sujatha Narayan ◽  
Brett D. Mensh ◽  
Florian Engert

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