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. 2017 Sep 13;118(5):2884–2889. doi: 10.1152/jn.00490.2017

Surface electrodes record and label brain neurons in insects

Konstantinos Kostarakos 1, Berthold Hedwig 2,✉
PMCID: PMC5680355  PMID: 28904103

We show that surface suction electrodes can be used to monitor the activity of auditory neurons in the cricket brain. They also allow delivering electrophoretically a fluorescent tracer to label the structure of the recorded neurons and the local neuropil to which the electrode was attached. This new extracellular recording and labeling technique is a versatile and useful method to explore neural processing in invertebrate sensory and motor systems.

Keywords: suction electrodes, single cell recordings, auditory neurons, brain, electrophoretic staining

Abstract

We used suction electrodes to reliably record the activity of identified ascending auditory interneurons from the anterior surface of the brain in crickets. Electrodes were gently attached to the sheath covering the projection area of the ascending interneurons and the ringlike auditory neuropil in the protocerebrum. The specificity and selectivity of the recordings were determined by the precise electrode location, which could easily be changed without causing damage to the tissue. Different nonauditory fibers were recorded at other spots of the brain surface; stable recordings lasted for several hours. The same electrodes were used to deliver fluorescent tracers into the nervous system by means of electrophoresis. This allowed us to retrograde label the recorded auditory neurons and to reveal their cell body and dendritic structure in the first thoracic ganglion. By adjusting the amount of dye injected, we specifically stained the ringlike auditory neuropil in the brain, demonstrating the clusters of cell bodies contributing to it. Our data provide a proof that surface electrodes are a versatile tool to analyze neural processing in small brains of invertebrates.

NEW & NOTEWORTHY We show that surface suction electrodes can be used to monitor the activity of auditory neurons in the cricket brain. They also allow delivering electrophoretically a fluorescent tracer to label the structure of the recorded neurons and the local neuropil to which the electrode was attached. This new extracellular recording and labeling technique is a versatile and useful method to explore neural processing in invertebrate sensory and motor systems.

suction electrodes are a well-established method to record the activity of peripheral nerves (Land et al. 2001; Stout 1971; Stout and Huber 1972) or to apply currents for electrical brain stimulation (Hedwig 1986, 1992; Johnson et al. 2007). As gentle low pressure is applied to the inner volume of the electrode, its tip is attached to the surface of a nerve or the cut end of a nerve is sucked into its opening for stable long-term extracellular recordings. Recently it has been shown that such electrodes can also be used to deliver fluorescent tracers into the nervous system, by means of electrophoresis (Isaacson and Hedwig 2017). Surprisingly, such electrodes have not been used to record neuronal activity from the surface of a ganglion or the brain. Here we employ suction electrodes to monitor the activity of auditory neurons in the brain of crickets, to characterize their response properties, and also to identify their structure and the organization of the neuropil at the recording site by electrophoretic dye injection. We thus provide a proof of principle that the use of surface electrodes is a versatile technique to analyze neural processing in small brains of model systems with little or no neurogenetic information available.

In crickets, the cell bodies and the dendrites of the ascending auditory interneurons AN1 and AN2 are located in the prothoracic ganglion while their axons ascend toward the brain, terminating in the ventral anterior protocerebrum (Wohlers and Huber 1982; Schildberger 1984). The structure of these neurons has been identified with intracellular recordings and staining. The spike activity of the AN1 and AN2 neurons has also been recorded with suction electrodes (Stout 1971; Stout and Huber 1972) and hook electrodes from the neck connectives (Hennig 1988; Kostarakos et al. 2008, 2009; Kostarakos and Römer 2010; Schmidt and Römer 2011). The AN1 auditory activity is tuned to around 5 kHz, corresponding to the frequency range of the cricket calling song, while the AN2 neuron acts within the context of bat detection and responds best to high-frequency signals in the range of 15–30 kHz. As AN2 has the larger axon diameter it stands out in such recordings whereas signals from the smaller AN1 axon are more difficult to obtain and sometimes require splitting the connective into axon bundles. A more simple way to record these neurons from the brain with an intact thoracic nervous system would be desirable for long-term recordings to study auditory processing and at the same time it would allow us to evaluate the recording technique for wider applications. Here we explored the use of surface suction electrodes to record auditory neurons ascending to the cricket brain and to identify these neurons by extracellular electrophoretic dye injection.

METHODS

Animals.

We used adult female bispotted field crickets (Gryllus bimaculatus) from a colony at the University of Graz, kept under established housing conditions for crickets. They had continuous access to water, fresh lettuce, and fish food.

Electrodes.

Tubes for suction electrodes were manually drawn under a dissecting microscope over a hot soldering iron from polycarbonate capillary tubing with 1.0 mm OD and 0.5 mm ID (Paradigm Optics, Vancouver, WA) to an outer diameter of 50–100 µm; tips were cut and heat polished. Electrodes were inserted into a custom-made electrode holder using a platinum wire as contact (Isaacson and Hedwig 2017). Its cavity was filled with a solution of 4% of Tylose (Tylose H200 YG4, ShinEtsu, Wiesbaden, Germany) dissolved in cricket saline with a composition (in g/l) of 8.6 NaCl, 0.74 KCl, 0.76 CaCl2, 2.38 HEPES. The electrode shaft was inserted and the lumen of the capillary was filled from the tip with 4% of Lucifer Yellow CH (Sigma-Aldrich, L0259) dissolved in aqueous 4% Tylose by applying a gentle suction to the holder cavity with a syringe, connected to the cavity via a flexible tube. Tylose was used to increase the viscosity of the solutions and prevented these from leaking out of the electrode.

Recordings.

For the recordings, specimens were tethered on a block of Plasticine fitted to a metal holder. The head capsule was opened frontally to expose the brain; it was rinsed with cricket saline to prevent the tissue from drying. A total of 38 female crickets were used to develop and test the method. The electrode tip was gently attached to the ventral surface of the brain where the ascending auditory interneurons AN1 and AN2 terminate. The tip position was altered until a good quality recording of AN1 or AN2 spike activity was obtained, and other sensory modalities were recorded at different surface areas of the brain. Good recordings could be obtained even without application of suction, when the electrode was slightly pushed onto the brain surface. The platinum reference electrode was placed into the saline next to the brain. Neuronal activity was amplified 1,000× and band-pass filtered between 300 Hz and 5 kHz with a differential amplifier (model 1700, A-M Systems, Carlsborg, WA). It was digitally recorded at a sampling rate of 21 kHz per channel using a CED Micro3-1401 controlled by Spike 2 software (Cambridge Electronics Design, Cambridge, UK). Experiments were performed at 28–32°C.

Sound stimuli.

Sound stimuli were computer generated with Cool Edit Pro 2000 (Syntrillium, Phoenix, AZ; now Adobe Audition) and were delivered at different intensities and frequencies via ultrasound magnetic speakers (MF1-S, Tucker Davis Technologies, Alachua, FL) controlled by a Tucker Davis attenuator system (PA5, Tucker Davis Technologies). Four sound pulses of 20-ms duration with 20-ms interpulse intervals were grouped in chirps of 140-ms duration and repeated every 460 ms. Other sensory stimuli were provided in a qualitative way by touching the appendages with a paintbrush or moving an object in front of the light source.

Staining.

After recording the auditory neurons, Lucifer yellow was injected into the brain at the recording site by hyperpolarizing DC current of −25 µA applied for 10 s to 5 min with a constant current source (Stimulus Isolator A-360, WPI, Sarasota, FL). Thereafter the dye was left to spread in the nervous system while the specimens were kept at 6°C° for 24 h. The central nervous system was dissected out from the brain to the first thoracic ganglion (TG1) and was fixed and cleared with standard histological techniques. Images of the stained neurons were taken with a Zeiss digital camera (AxioCamERc5s) attached to a Zeiss Axioplan (both Zeiss, Wetzlar, Germany) and compared against the structures of AN1, AN2 (Schildberger 1984; Schildberger et al. 1989), and local brain neurons (Kostarakos and Hedwig 2012; Schöneich et al. 2015).

Data analysis.

Representative recordings of neurons were selected with Spike 2 and processed in Neurolab (Knepper and Hedwig 1997; Römer et al. 2002), with an algorithm that calculated the overall voltage change in a gliding time window of 1.2 ms, corresponding to the duration of a spike, and thereby increased the signal-to-noise level in the filtered data. For quantitative analysis the timing of the filtered spikes was subsequently detected with a threshold filter and peristimulus-time (PST) histograms were calculated. The mean number of action potentials (AP) per chirp (AP/chirp) was calculated over a time window of 10–200 ms after the onset of a chirp.

RESULTS

Placing a suction electrode tip gently on to the ventral surface of the protocerebrum reliably recorded spike activity of underlying neurons. Single units of 50–200 µV amplitude could easily be discerned from a background noise of 20–30 µV. When the tip was positioned at different areas of the brain (Fig. 1A) it selectively picked up neural activity in response to, e.g., antennal stimulation, touching the front legs, or light stimuli. In this way the method allowed us to scan the surface of the brain for modality-specific responses and we obtained single-unit, as well as multiple-unit visual, antennal, and proprioceptive activity (Fig. 1, B and C). When the tip was positioned on the area of the protocerebrum where the ascending auditory neurons AN1 and AN2 terminate, their spike activity could reliably be recorded in response to repetitive acoustic stimuli. The quality of the recording could be improved by very gently pushing the electrode onto the brain or applying gentle suction, which sealed the tip onto the neurolemma. The recordings picked up simultaneously the combined activity of AN1 and AN2 or either neuron in a highly selective manner and could last unchanged for several hours.

Fig. 1.

Fig. 1.

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Neural activity recorded with a surface electrode placed at the ventral side of the brain. A: electrode positions at the ventral side of the brain for the different recordings. B: single-unit and multiunit responses obtained at different positions in response to acoustic pulse patterns, to changing light intensity; spikes elicited upon touching the ipsilateral antenna or the ipsilateral front leg with a paintbrush. C: the activity in response to sensory stimulation demonstrates the signal-to-noise ratio and the selectivity of the recording method. The timing of stimulus presentations is indicated by dots above the recordings.

Acoustic stimulation at 75 dB sound pressure level (SPL) allowed us to characterize the spike activity of the recorded neurons based on a quantitative analysis of their frequency tuning and PST histograms (Fig. 2). The activity patterns revealed two different spike amplitudes, with AN2 generally giving a larger response (Fig. 2A); the threshold for AN1 was around 43 dB SPL and for AN2 around 48 dB SPL. Typical responses of AN1 and AN2 were obtained with different stimulus frequencies, with AN1 neurons responding best to 5 kHz sound pulses, whereas AN2 neurons responded best in the high-frequency range of 15–40 kHz, as reflected in the frequency tuning curves (Fig. 2B). The PST histograms obtained in response to 5- and 20-kHz pulse patterns (Fig. 2, C and D) demonstrate a typical AN1 response coupled to the pulse pattern of the chirp with 20.0 ± 2.3 AP/chirp and a less strong response of 13.1 ± 1.3 AP/chirp for AN2. On average AN1 and AN2 responded with 24.9 ± 4.0 and 17.1 ± 3.9 AP/chirp, respectively (N = 6 for both neurons). Response latencies to the first sound pulse of a chirp were rather short and were on average 13.7 ± 3.0 ms for AN1 and 14.0 ± 1.2 ms for AN2, as experiments were performed at a high room temperature. These data demonstrated that the activity of identified auditory neurons and of other single units can be selectively recorded through the neuronal sheath from the surface of the intact brain.

Fig. 2.

Fig. 2.

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Recordings of AN1 and AN2 activity in response to sound pulses presented with different frequencies. A: the spike patterns of the auditory neurons clearly stand out from the background activity; the signal-to-noise ratio is increased by applying a gliding length filter, calculating the sum of amplitude changes over a time window of 1.2 ms. A switch in sound frequency from 20 to 5 kHz is accompanied by a shift in neuronal activity from AN2 to AN1. B: frequency tuning curves of the auditory activity in response to the acoustic stimuli give the characteristic responses of AN1 and AN2, at each frequency 5 pulses were presented (C and D). Neuronal activity and peristimulus-time (PST) histograms with a bin width of 5 ms, in response to chirp patterns presented at 5 or 20 kHz reveal the typical temporal activity patterns of AN1 and AN2. AP, action potentials.

We then explored whether this extracellular technique could also be used for labeling neurons at the recording site. Based on a recently reported electrophoretic staining method (Isaacson and Hedwig 2017) we used the electrodes to deliver the fluorescent tracer Lucifer yellow into the neural tissue below the opening of the electrode tip. The staining result depended on the amplitude and duration of the current applied. In experiments where auditory neurons were recorded, subsequent injection of Lucifer yellow reliably labeled the neurons with their cell bodies, neurites, and dendrites in the TG1, allowing us to identify the auditory neurons as AN1 and AN2 (Fig. 3A). Labeling the AN1 and AN2 structures in TG1 was successful in 12 of 14 staining attempts; in two unsuccessful cases two axons could be traced through the subesophageal ganglion (SEG) toward the TG1. When applying −25 µA for 3 min the dye injection overstained the brain, here cellular details were not discernible but the auditory neurons could be clearly revealed in TG1. Reducing the electrophoresis time to 15 s still was sufficient to identify the auditory neurons in the prothoracic ganglion and limited the spread of dye in the brain and labeled neurons just in the vicinity of the recording site (Fig. 3, B and C). In 11 experiments, staining in the brain reliably revealed structural details such as the ringlike branching pattern of local auditory neurons in the anterior protocerebrum. This is based on the axonal branching pattern of the AN1 neuron and the neurites of the local auditory neurons, aligned with these arborizations (Kostarakos and Hedwig 2012). Staining also revealed three clusters of cell bodies with their primary neurites projecting toward this structure (Fig. 3B). In three more selective stainings, the anterior cluster contained ~16 cell bodies, the lateral one ~13 and the posterior cluster ~25 cell bodies. These clusters match the position of cell bodies of identified auditory neurons involved in song pattern recognition (Kostarakos and Hedwig 2012; Schöneich et al. 2015). At the recording site of the auditory neuropil, the staining procedure was surprisingly selective for the ascending auditory neurons; only few other axons and neurons from the SEG were picked up as well. The surface electrodes thus not only allowed us to record and identify specific neurons, but local dye injection also revealed structural and organizational details of the surrounding neural tissue. The specific structures labeled depended on the precise location of the surface electrodes. Different details were highlighted in different experiments.

Fig. 3.

Fig. 3.

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Electrophoretic labeling of auditory neurons and brain neuropils with surface electrodes. A: characteristic structure of AN1 and AN2 with soma positions and dendrites in TG1, stained after their axon terminals in the brain were labeled with Lucifer yellow for 3 min. Inset shows structure of Lucifer yellow-stained AN1 and AN2 neurons in TG1, from Wohlers and Huber (1982) by permission. B and C: the ringlike arborization pattern of the ascending neurons and of local auditory neurons in the anterior protocerebrum revealed by electrophoretic injection of Lucifer yellow for 15 s. Labeled are three separate clusters of ventral cell bodies, with neurites connected to the ringlike arborization pattern. These clusters are positioned at the anterior protocerebrum (ant-C), the lateral protocerebrum (lat-C), and the lateral posterior protocerebrum (post-C). Insets show the projection and axonal arborizations of AN1 (B) and the structure of a local auditory brain neuron LN3 (C) labeled by intracellular staining; modified from Zorović and Hedwig (2011) and Kostarakos and Hedwig (2012).

DISCUSSION

Our approach of extracellular recording and labeling identified neurons is based on a method introduced by Isaacson and Hedwig (2017) and to our best knowledge has not been applied before in any invertebrate nervous system. We used surface electrodes to reliably record extracellularly the spike activity of identified ascending auditory neurons terminating ventrally in the brain of crickets and to reveal their thoracic structure by electrophoretic dye injection. Different sensory modalities could also be recorded at different locations on the brain surface, corresponding to the gross organization of neural processing in the brain.

Single or multichannel metal electrodes have been employed to study sensory and motor processing in the brain of cockroaches (Bender et al. 2010; Guo and Ritzmann 2013; Ritzman et al. 2008), grasshoppers (Bhavsar et al. 2015, 2017), bees (Brill et al. 2013), and rodent brain slices (Brown et al. 2006). As the multielectrodes come with a diameter of at least 20–40 μm some damage is unavoidable when these electrodes break through the sheath and penetrate the neural tissue, limiting the number of recording sites that can be probed. Although the electrode position can be labeled by depositing metal ions or fluorescent tracers, no information on the structure of the recorded neurons is obtained.

The method described here allows recording of neuronal activity at different brain sites without obvious damage to the tissue, and as a specific advantage neurons below the recording site can be labeled with fluorescent tracers. This new and surprising possibility of extracellular surface recordings also allows obtaining structural information on the recorded neurons and the local neuron populations. The method seems to be selective to fibers close to the recording site and in crickets allows easy recordings of ascending auditory neurons, which terminate close to the ventral surface of the brain (Schildberger 1984). We successfully tested the approach to monitor the activity of thoracic motoneurons in locusts and suggest that it can be applied to a wide range of invertebrate nervous systems. Neurons deeper in the brain or a ganglion may also be recorded when more gently force is applied to the electrode tip. This option was not yet systematically explored.

Our methodological approach was inspired by transdermal delivery of pharmaceuticals by iontophoresis (Rawat et al. 2008). It also allows the delivery of calcium-sensitive dyes into nerves and central neurons (Isaacson and Hedwig 2017) and is a new tool to study neural processing in insect nervous systems. With further technical refinement it may be combined with intracellular recordings or the local application of polar neuroactive substances. This offers new possibilities to study the activity and function of invertebrate nervous systems in species, in which genetically engineered calcium indicators are not yet available. Using large-scale surface electrodes with multiple contact points should allow simultaneous multichannel recordings to scan brain activity over a wider range and to simultaneously explore different neuropil regions and functions.

GRANTS

The work was supported by the Royal Society in a Newton International Fellowship alumni funding.

DISCLOSURES

No conflicts of interest, financial or otherwise, are declared by the authors.

AUTHOR CONTRIBUTIONS

K.K. and B.H. performed experiments; K.K. and B.H. analyzed data; K.K. and B.H. interpreted results of experiments; K.K. and B.H. prepared figures; K.K. and B.H. drafted manuscript; K.K. and B.H. edited and revised manuscript; K.K. and B.H. approved final version of manuscript; B.H. conceived and designed research.

ACKNOWLEDGMENTS

B. Hedwig visited the former Newton fellow K. Kostarakos as an external collaborator. We are grateful to H. Römer for constructive comments on the work.

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