Differential Receptive Field Properties of Parvalbumin and Somatostatin Inhibitory Neurons in Mouse Auditory Cortex

Abstract

Cortical inhibitory circuits play important roles in shaping sensory processing. In auditory cortex, however, functional properties of genetically identified inhibitory neurons are poorly characterized. By two-photon imaging-guided recordings, we specifically targeted 2 major types of cortical inhibitory neuron, parvalbumin (PV) and somatostatin (SOM) expressing neurons, in superficial layers of mouse auditory cortex. We found that PV cells exhibited broader tonal receptive fields with lower intensity thresholds and stronger tone-evoked spike responses compared with SOM neurons. The latter exhibited similar frequency selectivity as excitatory neurons. The broader/weaker frequency tuning of PV neurons was attributed to a broader range of synaptic inputs and stronger subthreshold responses elicited, which resulted in a higher efficiency in the conversion of input to output. In addition, onsets of both the input and spike responses of SOM neurons were significantly delayed compared with PV and excitatory cells. Our results suggest that PV and SOM neurons engage in auditory cortical circuits in different manners: while PV neurons may provide broadly tuned feedforward inhibition for a rapid control of ascending inputs to excitatory neurons, the delayed and more selective inhibition from SOM neurons may provide a specific modulation of feedback inputs on their distal dendrites.

A Feedforward Inhibitory Circuit Mediates Lateral Refinement of Sensory Representation in Upper Layer 2/3 of Mouse Primary Auditory Cortex

“…We used agar (3.25%) to minimize cortical pulsation. Neurons recorded at 375-500 m below the pial surface were analyzed for L4 and 150 -250 m for upper L2/3 (Kaur et al, 2005;Oviedo et al, 2010). A small number of cells recorded at depths between 250 and 350 m were analyzed as lower L2/3 cells.…”

“…The observed TRF refinement in the upper L2/3 could possibly be attributable to excessive cortical inhibition (Ojima and Murakami, 2002;Sadagopan and Wang, 2010;O'Connell et al, 2011;Zhang et al, 2011a), which has sometimes been measured as the effectiveness of suppressing spikes. Following previous studies (Sutter and Loftus, 2003;, we evaluated inhibitory regions in the frequency-intensity space with a two-tone stimulation paradigm, which consisted of a CF tone preceded by a testing tone with various combinations of frequency and intensity (see Materials and Methods).…”

“…For example, in the primate auditory cortex, a large proportion of superficial neurons exhibit enclosed receptive fields, which are strongly selective for sound intensity (Sadagopan and Wang, 2010). In the mouse visual cortex, oriented simple-cell receptive field structures are more pronounced in L2/3 Ma et al, 2010), and selectivity for stimulus size is strengthened by specific inhibitory inputs from L2/3 (Adesnik et al, 2012). Compared with the input layer, L2/3 circuits are also found more susceptible to changes induced by alterations of the animal's sensory experience (Trachtenberg et al, 2000;Allen et al, 2003), indicating that the superficial layers play an important role in adapting cortical functions to the external environment.…”

“…Conversely, it has been shown in some species that superficial layers contain elaborate horizontal axons (Gilbert and Wiesel, 1983;Callaway and Katz, 1990;White et al, 2001;Marino et al, 2005). The horizontal connections may provide a way of modulating functional responses of neurons in a context-dependent manner (Blakemore and Tobin, 1972;Nelson and Frost, 1978;Allman et al, 1985;Gilbert and Wiesel, 1990;Knierim and van Essen, 1992;Levitt and Lund, 1997;Walker et al, 1999), determine the spatial summation of neuronal responses (Hubel and Wiesel, 1965;Sillito and Versiani, 1977;DeAngelis et al, 1994;Li and Li, 1994;Adesnik et al, 2012), or even help to create novel functional properties (Chisum et al, 2003). To understand the logic for hierarchical cortical processing, it is important to elucidate excitatory and inhibitory synaptic circuit mechanisms underlying specific laminar processing.…”

Memory formation and retrieval of neuronal silencing in the auditory cortex

“…Inhibitory interneurons in the auditory cortex probably silence neighboring excitatory neurons in a frequency-dependent manner and then contribute to behavioral expression. Indeed, parvalbumin-and somatostatin-expressing inhibitory neurons in the auditory cortex are well-tuned for frequency of tones (16,17). Moreover, electrophysiological stimulation of putative inhibitory neurons in the somatosensory cortex affects behavioral responses in a mouse's detection task (18,19).…”