Neuronal Activity of Mitral-Tufted Cells in Awake Rats During Passive and Active Odorant Stimulation

Abstract

Fuentes RA, Aguilar MI, Aylwin ML, Maldonado PE. Neuronal activity of mitral-tufted cells in awake rats during passive and active odorant stimulation. J Neurophysiol 100: 422-430, 2008. First published May 21, 2008 doi:10.1152/jn.00095.2008. Odorants induce specific modulation of mitral/tufted (MT) cells' firing rate in the mammalian olfactory bulb (OB), inducing temporal patterns of neuronal discharge embedded in an oscillatory local field potential (LFP). While most studies have examined anesthetized animals, little is known about the firing rate and temporal patterns of OB single units and population activity in awake behaving mammals. We examined the firing rate and oscillatory activity of MT cells and LFP signals in behaving rats during two olfactory tasks: passive exposure (PE) and two-alternative (TA) choice discrimination. MT inhibitory responses are predominant in the TA task (76.5%), whereas MT excitatory responses predominate in the PE task (59.2%). Rhythmic discharge in the 12-to 100-Hz range was found in 79.0 and 68.9% of MT cells during PE and TA tasks, respectively. Most odorants presented in PE task increase rhythmic discharges at frequencies Ͼ50 Hz, whereas in TA, one of four odorants produced a modest increment Ͻ40 Hz. LFP oscillations were clearly modulated by odorants during the TA task, increasing their oscillatory power at frequencies centered at 20 Hz and decreasing power at frequencies Ͼ50 Hz. Our results indicate that firing rate responses of MT cells in awake animals are behaviorally modulated with inhibition being a prominent feature of this modulation. The occurrence of oscillatory patterns in single-and multiunitary discharge is also related to stimulation and behavioral context, while the oscillatory patterns of the neuronal population showed a strong dependence on odorant stimulation.

Balancing the Robustness and Efficiency of Odor Representations during Learning

“…On average, 41.6 ± 7.5 % of the imaged mitral cell population exhibited significant changes in fluorescence to at least one odorant during the odor period. The odorant responses included both increases and decreases in fluorescence (Day 1, 72.3 ± 9.0 % of responses were increases and 27.7 ± 9.0 % were decreases; Day 7, 72.2 ± 7.0 % of responses were increases and 27.8 ± 7.0 % were decreases), consistent with previous reports (Bathellier et al, 2008; Davison and Katz, 2007; Doucette and Restrepo, 2008; Fuentes et al, 2008; Gschwend et al, 2012; Kato et al, 2012; Kollo et al, 2014; Li et al, 2015; Nagayama et al, 2004; Rinberg and Gelperin, 2006; Shusterman et al, 2011; Yokoi et al, 1995). Additionally, a large fraction of the responsive mitral cells exhibited divergent responses between the two odorants on Day 1 (Figures 2B-D and Figure S1).…”

The Olfactory System

“…Spontaneous firing rates in awake rodents are generally similar to that in anesthetized preparations; range, 1-33 Hz, mean range, 12-17 Hz (Kay and Laurent, 1999;Fuentes et al, 2008;Shusterman et al, 2011). However, in one study MTCs exhibited a large drop in firing from ∼27 to 9 Hz after anesthesia (Rinberg et al, 2006).…”

Beta and gamma oscillatory activities associated with olfactory memory tasks: different rhythms for different functional networks?

“…When exposed to a neutral unfamiliar odorant, only weak beta oscillations are observed but their amplitude increases through training as soon as this odor starts to acquire a behavioral meaning for the animal (Ravel et al, 2003; Martin et al, 2004b). Such a learning-induced increase in beta power has been observed in several structures associated with odor processing (MOB, PCx, entorhinal cortex, and hippocampus) and for a variety of behavioral paradigms (see Table 1): Go/No-Go task (Ravel et al, 2003; Martin et al, 2004b, 2007; Gourévitch et al, 2010; Lepousez and Lledo, 2013), two-alternative choice task (Fuentes et al, 2008) and aversive learning (Chapuis et al, 2009). However, a few studies, with similar operant conditioning, report an odor evoked gamma increase instead of a change in beta activity (Beshel et al, 2007; Rosero and Aylwin, 2011).…”

“…Besides the difficulty of the task, we can make the hypothesis that these two tasks involve different strategies and thus activate different brain circuits. In the two-alternative choice paradigm, odors can elicit high amplitude beta oscillations (10–30 Hz) and a significant decrease in the gamma band (70–100 Hz) (Fuentes et al, 2008). However, Beshel et al (2007) using this task to compare successive odor pairs discriminations obtained different results.…”