Chem. Senses 26: 585-594,
2001
© Oxford University Press 2001
SYMPOSIUM: AChemS XXII Symposium |
Neuromodulation and the Functional Dynamics of Piriform Cortex
Department of Neurobiology and Behavior, Cornell University, 245 Seeley G. Mudd Hall, Ithaca, NY 14853 and 1 Department of Psychology, Program in Experimental and Computational Neuroscience and Center for BioDynamics, Boston University, 64 Cummington Street, Boston, MA 02215, USA
Correspondence to be sent to: Christiane Linster, Department of Neurobiology and Behavior, Cornell University, 245 Seeley G. Mudd Hall, Ithaca, NY 14853, USA. e-mail: cl224{at}cornell.edu
Abstract
Acetylcholine and norepinephrine have a number of effects at the cellular level in the piriform cortex. Acetylcholine causes a depolarization of the membrane potential of pyramidal cells and interneurons, and suppresses the action potential frequency accommodation of pyramidal cells. Acetylcholine also has strong effects on synaptic transmission, suppressing both excitatory and inhibitory synaptic transmission. At the same time as it suppresses synaptic transmission, acetylcholine enhances synaptic modification, as demonstrated by experiments showing enhancement of long-term potentiation. Norepinephrine has similar effects. In this review, we discuss some of these different cellular effects and provide functional proposals for these individual effects in the context of the putative associative memory function of this structure.
Introduction
Numerous anatomical studies have described the structure of the olfactory system [for a review see Haberly (Haberly, 1985
)]. Anatomical data demonstrate neuromodulatory innervation of these regions, including cholinergic and GABAergic innervation arising from the horizontal limb of the diagonal band (HDB) (Luskin and Price, 1982; Brashear et al., 1986; Zaborszky et al., 1986) and noradrenergic innervation arising from the locus coeruleus (McLean et al., 1989) [for a review see Shipley and Ennis (Shipley and Ennis, 1996)].
A number of studies have shown an important role for neuromodulatory effects in olfactory memory function. These include data showing impairments of odor memory induced by the muscarinic cholinergic antagonist scopolamine, as well as lesions of the cholinergic and GABAergic neurons in the HDB (Hunter and Murray, 1989; Ravel et al., 1992, 1994; Paolini and McKenzie, 1993, 1996; Roman et al., 1993). In addition, numerous studies have shown the importance of norepinephrine for olfactory learning (Pissonnier et al., 1985; Rosser and Keverne, 1985; Brennan et al., 1990; Guan et al., 1993; Sullivan et al., 1989, 1991, 1992).
Here we provide a review of physiological data on cellular effects of these neuromodulators, a description of computational models analyzing the behavioral role of these neuromodulators, and some behavioral data testing hypotheses derived from these computational models. The piriform cortex provides an excellent region for analysis of neuromodulatory effects, as its structure resembles a class of neural network models termed ‘associative memories’ (Haberly, 1985; Haberly and Bower, 1989; Hasselmo et al., 1990). This provides a clear computational framework for analyzing the functional role of the changes in network dynamics induced by neuromodulatory agents (Figure 1).
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Studying neuromodulatory effects in olfactory cortex
Acetylcholine and norepinephrine have a number of effects at the cellular level in the piriform cortex. Acetylcholine causes a depolarization of the membrane potential of pyramidal cells (Tseng and Haberly, 1989; Barkai and Hasselmo, 1994) and interneurons (Gellman and Aghajanian, 1993), and suppresses the spike frequency accommodation of pyramidal cells (Tseng and Haberly, 1989; Barkai and Hasselmo, 1994), as well as increasing the excitability of olfactory cortex cells in vivo (Zimmer et al., 1999). Like norepinephrine, acetylcholine also has strong effects on synaptic transmission, suppressing both excitatory synaptic transmission (Collins et al., 1984; McIntyre and Wong, 1986; Williams and Constanti, 1988; Hasselmo and Bower, 1992; Hasselmo et al., 1997; Linster et al., 1999) and inhibitory synaptic transmission (Patil and Hasselmo, 1999). At the same time as it suppresses synaptic transmission, acetylcholine enhances synaptic modification, as demonstrated by experiments showing enhancement of long-term potentiation (Hasselmo and Barkai, 1995; Patil et al., 1998). In this review, we discuss some of these different cellular effects and provide functional proposals for them in the context of the putative associative memory function of this structure.
Selective cholinergic suppression of excitatory synaptic transmission
The piriform cortex is an excellent structure for studying the neuromodulation of synaptic transmission, as it has a clear laminar segregation of different types of synapses. As shown in Figure 1, the afferent fibers arising from the olfactory bulb terminate in the most superficial layer of piriform cortex, layer Ia, whereas the fibers arising from other pyramidal cells within the cortex terminate in the deeper layers, including layers Ib and III. Cutting brain slices perpendicular to the surface of the cortex allows separate stimulation of synaptic potentials in the two layers, with stimulating electrodes in layer Ia or Ib (Figure 2). Recording can take place either intracellularly, from the pyramidal cell bodies tightly clustered in layer II, or extracellularly, from the layer being stimulated.
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Previous research had demonstrated cholinergic modulation of excitatory transmission in tangential slices of the piriform cortex (Williams and Constanti, 1988
). However, the use of transverse slices allowed demonstration of striking differences in the effect of neuromodulators on the different synaptic pathways. As shown in Figure 3A (Hasselmo and Bower, 1992), perfusion of acetylcholine through the slice chamber causes a suppression of synaptic potentials elicited with stimulation in layer Ib (intrinsic fibers) while having a weaker effect on synaptic potentials elicited with stimulation in layer Ia (afferent fibers). This selectivity is supported by additional studies performed in vivo (Figure 3B), showing that stimulation of the horizontal limb of the diagonal band causes suppression of synaptic potentials evoked with stimulation in caudal piriform cortex and entorhinal cortex, which presumably activates primarily intrinsic fibers (Linster et al., 1999). In contrast, stimulation of the horizontal limb actually enhances potentials elicited by stimulation of afferent input fibers in the lateral olfactory tract (Linster et al., 1999) (Figure 3C).
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t = 50 ms). The population EPSP observed in layer Ia of the PC after stimulation of the LOT has a first negative peak (A1), followed by a second negative inflection (B1). A1 is generated by the monosynaptic EPSP in layer Ia and B1 is thought to reflect the disynaptic EPSP due to activation of the intrinsic fibers within the piriform cortex. At 50 ms after the tetanus in the HDB, component B1 is greatly enhanced. There is no effect on the monosynaptic component A1. Each trace is the average of 10 stimulations. The lines with arrows to the left of the potential indicate the measurements of the amplitude of the A1 and B1 components used for the analysis. Graph on the right side: responses to the baseline pulse and the test pulse 50 ms after HDB stimulation and 30 min after the injection of 0.5 mg/kg scopolamine. Scopolamine abolishes or greatly reduces the enhancement of component B1 after HDB stimulation. Each trace is the average of 10 stimulations. A and B are from the same animal. (C) Effect of stimulation of the HDB on the population EPSP in layer Ia in response to stimulation of layers II–III in the posterior piriform cortex recorded in vivo. Graph on the left side: responses to the baseline pulse (baseline response) and the test pulse 50 ms after HDB stimulation (The cholinergic suppression of excitatory transmission might appear somewhat paradoxical, as acetylcholine has been shown to be important for learning. Why would a substance that is important for learning cause suppression of excitatory transmission? The importance of this selective suppression of transmission has been analyzed in computational models, and recent experiments have tested behavioral predictions of these computational models. Here we will first describe the behavioral experiment, and then show a schematic model of how suppression of transmission could play a role in this experiment.
The basic experiment is shown in Figure 4. The experiment tested the learning of odor pairs presented at separate odor ports. Initially, the rat must learn to respond to odor A when presented with the odor pair A–B. Then, in a separate phase of the experiment, the rat must learn to respond to odor C when presented with odor pair A–C, and during the same period must learn to respond to odor D when presented with odor pair D–E. In a counterbalanced design, rats received injections of scopolamine, methylscopolamine or saline after learning of A–B and before learning of A–C and D–E. This allowed analysis of how scopolamine influenced the learning of overlapping odor pairs (A–C) versus non-overlapping odor pairs (D–E).
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This behavioral task was designed to test hypotheses arising from computational models of the piriform cortex (Hasselmo and Bower, 1992
). The basic hypothesis is demonstrated in Figure 5. Figure 5A demonstrates the putative mechanisms for encoding the correct response to individual odor pairs. When presented with odor pair A–B, the response to odor A is rewarded. This association between the odor pair and the correct response can be encoded as strengthened synaptic connections between the population of neurons representing these two odors and the population of neurons activated during the response to odor A. The strengthening of synapses follows a Hebb rule, in which synapses are only strengthened in the presence of both pre- and post-synaptic activity. A direct association between activity evoked by sensory input and that evoked by motor responses is possible in the piriform cortex, as it has been shown that select populations of neurons in the piriform cortex fire during multiple different components of odor discrimination tasks, including odor sampling and response generation (Schoenbaum and Eichenbaum, 1995). Once this association has been encoded, the next time the odor pair is encountered, activity will spread along the previously strengthened connections, allowing activation of the response to odor A for correct retrieval.
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This association works well for single odor pairs, but can run into difficulties of proactive interference for overlapping odor pairs. As illustrated in Figure 5B, if the rat has been trained to respond to odor A in the pair A–B, then it could be more difficult to train the rat to respond to odor C in odor pair A–C. This problem of proactive interference arises because the presentation of odor A causes activity to spread along previously modified synapses to activate the previously learned response to odor A. This can result in incorrect responses, and undesired encoding of an association between odor C and the response to odor A. Thus, transmission across previously modified synapses interferes with the encoding of a new response.
Figure 5C shows how the selective cholinergic suppression of excitatory synaptic transmission can prevent this difficulty. Recall that acetylcholine does not suppress afferent input from the olfactory bulb. Thus, during encoding of odor pair A–C, acetylcholine does not block the sensory input activity. However, it does block the spread of activity along excitatory intrinsic connections within the cortex, preventing interference due to activation of the previous response to odor A. With this suppression of previous retrieval, the network can more effectively encode the new response to odor C. Thus, comparison of Figures 5B and 5C shows the prediction for effects of scopolamine in this experiment. Scopolamine will block effects of acetylcholine on intrinsic synaptic transmission, enhancing the type of proactive interference illustrated in Figure 5B.
The results of the experiment support this hypothesis, as shown in Figure 6 (De Rosa and Hasselmo, 2000). Injections of scopolamine caused a stronger impairment of the ability to respond to odor C in the overlapping odor pair A–C, in comparison to its weaker impairment of the ability to respond to odor D in the non-overlapping odor pair D–E. Thus, scopolamine appears to enhance proactive interference, consistent with its blockade of the cholinergic suppression of excitatory synaptic transmission at intrinsic synapses in the piriform cortex. This model is further supported by experimental data showing that electrical stimulation of the olfactory cortex can modulate the activity of neurons in the HDB, thus providing a pathway for regulation of cholinergic activity (Linster and Hasselmo, 2000) (Figure 7). Similar effects have been obtained in an experiment performed in human subjects, in which scopolamine caused greater impairments in the encoding of overlapping versus non-overlapping word pairs (Kirchhoff et al., 2000).
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Cholinergic modulation of long-term potentiation
To prevent interference, the suppression of excitatory synaptic transmission should take place during the encoding of new information. This strict temporal correlation of suppressed transmission and modification can be obtained if the same modulator causes suppression of transmission and enhancement of synaptic modification. Experimental data support this role for acetylcholine. In addition to the suppression of transmission described above (Hasselmo and Bower, 1992; Linster et al., 1999), acetylcholine causes enhancement of long-term potentiation in the piriform cortex (Hasselmo and Barkai, 1995; Patil et al., 1998).
This was initially shown (Hasselmo and Barkai, 1995) by studying the effect of 5 Hz stimulation in two conditions: (i) during continuous infusion of the cholinergic agonist carbachol (CCh) and (ii) during perfusion of normal ACSF (artificial cerebrospinal fluid). A larger magnitude of long-term potentiation was obtained when the stimulation took place during cholinergic modulation. An example of data from this study is shown in Figure 8. This enhancement of long-term potentiation could result from a number of different effects of cholinergic modulation, including the depolarization of pyramidal cells and the suppression of spike frequency accommodation. Spike frequency accommodation occurs in piriform cortex pyramidal cells in response to long current injections. During the current injection, neurons initially fire spikes at a high frequency, which gradually decreases until spiking stops later in the injection due to activation of calcium-sensitive potassium currents. Cholinergic modulation suppresses the calcium-sensitive potassium current, allowing a more sustained spiking response to current injection. In computational models, this enhanced spiking response causes greater post-synaptic depolarization, which enhances the activation of NMDA receptors and the rate of Hebbian synaptic modification.
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This enhancement of long-term potentiation would be particularly effective if it applied to dendrites on which there is a convergence of afferent input and active intrinsic synapses. This would enhance the accuracy of encoding of new afferent input. Experiments in our laboratory have demonstrated that cholinergic modulation enables associative long-term potentiation (Patil et al., 1998
) between the afferent fibers and the intrinsic association fibers (Figure 9A). In these experiments, a strong stimulation was presented to layer Ia of the piriform cortex (bursts of four pulses at 100 Hz at 200 ms intervals). This tetanic stimulation was accompanied by a weaker stimulation in layer Ib, given at 5 Hz between the second and third pulse of the four pulse burst in layer Ia (Figure 9B). Under both normal saline or CCh, neither the tetanus in layer Ia nor the weak stimulation alone produced changes in the population excitatory post-synaptic potential (EPSP) observed in response to stimulation of layer Ib. However, under bath application of 50 µM CCh, the pairing of the weak stimulation in layer Ib with the tetanic stimulation in layer Ia produced a significant increase of the population EPSP in response to layer Ib stimulation (Figure 10).
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50% of the maximal response. After bath application of CCh, the response amplitude to test stimuli decreased and stabilized after In previous work, this enhancement of associative long-term potentiation was obtained with selective blockade of inhibitory synaptic transmission (Kanter and Haberly, 1993
). Cholinergic modulation could provide this same effect through modulation of inhibitory synaptic potentials. Recordings from piriform cortex pyramidal cells have demonstrated cholinergic modulation of inhibitory synaptic potentials, as illustrated in Figure 11 (Patil and Hasselmo, 1999). In these experiments, perfusion of the cholinergic agonist CCh caused suppression of inhibitory synaptic potentials recorded with sharp electrode techniques as well as inhibitory synaptic currents recorded with whole cell patch clamp (Patil and Hasselmo, 1999). This modulation of inhibitory transmission appears to be stronger for transmission in layer Ib than for that in layer Ia.
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Noradrenergic modulation in the piriform cortex
Noradrenergic modulation appears to have some effects similar to those of acetylcholine, providing a similar enhancement of the network response to external afferent input relative to intrinsic transmission. In particular, noradrenergic modulation causes selective suppression of excitatory intrinsic synaptic transmission, as shown in Figure 12 (Hasselmo et al., 1997).
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Network simulations demonstrate that the noradrenergic suppression of transmission could result in an enhancement of response to afferent input relative to internal activity. This can be referred to as enhanced signal-to-noise ratio— an effect that has been studied in a number of other cortical regions (Sara, 1985
; Servan-Schreiber et al., 1990). Simulations of the piriform cortex illustrate how modulation of synaptic transmission influences the response to afferent input, as shown in Figure 13. Thus, the net effects of norepinephrine may result in enhanced encoding of sensory input. This could provide cellular mechanisms for the important role of norepinephrine observed in early olfactory learning [reviewed by Sullivan et al. (Sullivan et al., 1992)].
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Summary
In summary, the piriform cortex provides an excellent structure for analysis of neuromodulatory effects on cortical processing, allowing analysis of selective effects on excitatory and inhibitory synaptic transmission, and computational modeling of these effects in the framework of associative memory function. This allows explanation of some existing behavioral data on cholinergic and noradrenergic modulation, and generation of further hypotheses to guide additional behavioral experiments.
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