Abstract
Layer 4 (L4) of primary auditory cortex (A1) receives a tonotopically organized projection from the medial geniculate nucleus of the thalamus. However, individual neurons in A1 respond to a wider range of sound frequencies than would be predicted by their thalamic input, which suggests the existence of cross-frequency intracortical networks. We used laser scanning photostimulation and uncaging of glutamate in brain slices of mouse A1 to characterize the spatial organization of intracortical inputs to L4 neurons. Slices were prepared to include the entire tonotopic extent of A1. We find that L4 neurons receive local vertically organized (columnar) excitation from layers 2 through 6 (L6) and horizontally organized excitation primarily from L4 and L6 neurons in regions centered ~300–500 μm caudal and/or rostral to the cell. Excitatory horizontal synaptic connections from layers 2 and 3 were sparse. The origins of horizontal projections from L4 and L6 correspond to regions in the tonotopic map that are approximately an octave away from the target cell location. Such spatially organized lateral connections may contribute to the detection and processing of auditory objects with specific spectral structures.
Highlights
IntroductionThese objects often contain component frequencies that are spectrally discontinuous and distributed across most of the hearing range
Sensory systems detect, identify, and track objects in the environment
We used laser-scanning photostimulation (LSPS) with glutamate uncaging to map the spatial location of cortical neurons that are presynaptic to Layer 4 (L4) neurons in A1
Summary
These objects often contain component frequencies that are spectrally discontinuous and distributed across most of the hearing range. This presents a problem for auditory processing because reassembling sounds as objects rather than as individual component frequencies requires that some auditory neurons integrate sensory activity over broad spatial ranges, which is not readily accomplished with spatially restricted local circuits. Most (but not all) pathways in the auditory brainstem and midbrain retain the tonotopically-organized narrow frequency representation that arises in the cochlea. Previous studies have suggested that extensive cross-frequency excitatory connectivity occurs within the primary auditory cortex (A1), and this may be one site in the auditory pathway where such cross-frequency convergence is necessary to begin to assemble auditory objects from the neural representation of sound. The organization of these circuits is not well understood
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